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2023 Volume 2
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Research progress on the relationship between rice protein content and cooking and eating quality and its influencing factors

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  • Received: 25 July 2023
    Accepted: 07 October 2023
    Published online: 27 October 2023
    Seed Biology  2 Article number: 16 (2023)  |  Cite this article
  • Proteins, the second-largest storage substance in rice endosperm, play an important role in determining the cooking and eating qualities of rice. Its contents are influenced by both genetic and environmental factors. This article provides a review of the evaluation methods for cooking and eating qualities of rice and starch physicochemical properties, the factors that affect the protein content of rice, the genetic basis of rice protein content, the research progress made in the genetic improvement of rice protein content, and the prospects for the future, aiming to provide a reference for the genetic improvement of rice protein content and the breeding of rice varieties with excellent taste.
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  • [1]

    Zhou H, Xia D, He Y. 2020. Rice grain quality—traditional traits for high quality rice and health-plus substances. Molecular Breeding 40:1

    doi: 10.1007/s11032-019-1080-6

    CrossRef   Google Scholar

    [2]

    Tian Y, Zhou Y, Gao G, Zhang Q, Li Y, et al. 2023. Creation of Two-Line Fragrant Glutinous Hybrid Rice by Editing the Wx and OsBADH2 Genes via the CRISPR/Cas9 System. International Journal of Molecular Sciences 24:849

    doi: 10.3390/ijms24010849

    CrossRef   Google Scholar

    [3]

    Zhang J, Zhang H, Botella J, Zhu J-K. 2018. Generation of new glutinous rice by CRISPR/Cas9-targeted mutagenesis of the Waxy gene in elite rice varieties. Journal of Integrative Plant Biology 60:369−75

    doi: 10.1111/jipb.12620

    CrossRef   Google Scholar

    [4]

    Xu Y, Lin Q, Li X, Wang F, Chen Z, et al. 2021. Fine-tuning the amylose content of rice by precise base editing of the Wx gene. Plant Biotechnology Journal 19:11−13

    doi: 10.1111/pbi.13433

    CrossRef   Google Scholar

    [5]

    Huang L, Li Q, Zhang C, Chu R, Gu Z, et al. 2020. Creating novel Wx alleles with fine-tuned amylose levels and improved grain quality in rice by promoter editing using CRISPR/Cas9 system. Plant Biotechnology Journal 18:2164−66

    doi: 10.1111/pbi.13391

    CrossRef   Google Scholar

    [6]

    Zhang Q, Zhang S, Yu X, Wei X, Huang X, et al. 2022. Fine-tuning grain amylose contents by genome editing of Waxy cis-regulatory region in rice. Molecular Breeding 42

    doi: 10.1007/s11032-022-01342-4

    CrossRef   Google Scholar

    [7]

    Liu X, Ding Q, Wang W, Pan Y, Tan C, et al. 2021. Targeted deletion of the first intron of the Wx b allele via CRISPR/Cas9 significantly increases grain amylose content in rice. Rice 15:1

    doi: 10.1186/s12284-021-00548-y

    CrossRef   Google Scholar

    [8]

    Zhou H, Xia D, Zhao D, Li Y, Li P, et al. 2021. The origin of Wx la provides new insights into the improvement of grain quality in rice. Journal of Integrative Plant Biology 63:878−88

    doi: 10.1111/jipb.13011

    CrossRef   Google Scholar

    [9]

    Zhang C, Yang Y, Chen S, Liu X, Zhu J, et al. 2020. A rare Waxy allele coordinately improves rice eating and cooking quality and grain transparency. Journal of Integrative Plant Biology 63:889−901

    doi: 10.1111/jipb.13010

    CrossRef   Google Scholar

    [10]

    Zeng D, Yan M, Wang Y, Liu X, Qian Q, et al. 2007. Du1, encoding a novel Prp1 protein, regulates starch biosynthesis through affecting the splicing of Wx b pre-mRNAs in rice (Oryza sativa L.). Plant Molecular Biology 65:501−9

    doi: 10.1007/s11103-007-9186-3

    CrossRef   Google Scholar

    [11]

    Isshiki M, Matsuda Y, Takasaki A, Wong HL, Satoh H, Shimamoto K. 2008. Du3, a mRNA cap-binding protein gene, regulates amylose content in Japonica rice seeds. Plant Biotechnology 25:483−87

    doi: 10.5511/plantbiotechnology.25.483

    CrossRef   Google Scholar

    [12]

    Cai Y, Zhang W, Fu Y, Shan Z, Xu J, et al. 2022. Du13 encodes a C2H2 zinc-finger protein that regulates Wx b pre-mRNA splicing and microRNA biogenesis in rice endosperm. Plant Biotechnology Journal 20:1387−401

    doi: 10.1111/pbi.13821

    CrossRef   Google Scholar

    [13]

    Wu YP, Pu CH, Lin HY, Huang HY, Huang YC, et al. 2014. Three novel alleles of FLOURY ENDOSPERM2 (FLO2) confer dull grains with low amylose content in rice. Plant Science 233:44−52

    doi: 10.1016/j.plantsci.2014.12.011

    CrossRef   Google Scholar

    [14]

    Takemoto-Kuno Y, Mitsueda H, Suzuki K, Hirabayashi H, Ideta O, et al. 2015. qAC2, a novel QTL that interacts with Wx and controls the low amylose content in rice (Oryza sativa L.). Theoretical and Applied Genetics 128:563−73

    doi: 10.1007/s00122-014-2432-6

    CrossRef   Google Scholar

    [15]

    Zhang H, Zhou L, Xu H, Wang L, Liu H, et al. 2019. The qSAC3 locus from indica rice effectively increases amylose content under a variety of conditions. BMC Plant Biology 19:275

    doi: 10.1186/s12870-019-1860-5

    CrossRef   Google Scholar

    [16]

    Igarashi H, Ito H, Shimada T, Kang DJ, Hamada S. 2021. A novel rice dull gene, LowAC1, encodes an RNA recognition motif protein affecting Waxy b pre-mRNA splicing. Plant Physiology and Biochemistry 162:100−9

    doi: 10.1016/j.plaphy.2021.02.035

    CrossRef   Google Scholar

    [17]

    Jin SK, Xu LN, Leng YJ, Zhang MQ, Yang QQ, et al. 2023. The OsNAC24-OsNAP protein complex activates OsGBSSI and OsSBEI expression to fine-tune starch biosynthesis in rice endosperm. Plant Biotechnology Journal 21:2224−40

    doi: 10.1111/pbi.14124

    CrossRef   Google Scholar

    [18]

    Wang J, Chen Z, Zhang Q, Meng S, Wei C. 2020. The NAC transcription factors OsNAC20 and OsNAC26 regulate starch and storage protein synthesis. Plant Physiology 184:1775−91

    doi: 10.1104/pp.20.00984

    CrossRef   Google Scholar

    [19]

    Bello BK, Hou Y, Zhao J, Jiao G, Wu Y, et al. 2019. NF-YB1-YC12-bHLH144 complex directly activates Wx to regulate grain quality in rice (Oryza sativa L.). Plant Biotechnology Journal 17:1222−35

    doi: 10.1111/pbi.13048

    CrossRef   Google Scholar

    [20]

    Zhang H, Xu H, Feng M, Zhu Y. 2018. Suppression of OsMADS7 in rice endosperm stabilizes amylose content under high temperature stress. Plant Biotechnology Journal 16:18−26

    doi: 10.1111/pbi.12745

    CrossRef   Google Scholar

    [21]

    Feng T, Wang L, Li L, Liu Y, Chong K, et al. 2022. OsMADS14 and NF-YB1 cooperate in the direct activation of OsAGPL2 and Waxy during starch synthesis in rice endosperm. New Phytologist 234:77−92

    doi: 10.1111/nph.17990

    CrossRef   Google Scholar

    [22]

    Zhu Y, Cai XL, Wang ZY, Hong MM. 2003. An Interaction between a MYC protein and an EREBP protein is involved in transcriptional regulation of the rice Wx gene. The Journal of Biological Chemistry 278:47803−11

    doi: 10.1074/jbc.M302806200

    CrossRef   Google Scholar

    [23]

    Yang D, Wu LY, Hwang Y-S, Chen LF, Huang N. 2001. Expression of the REB transcriptional activator in rice grains improves the yield of recombinant proteins whose genes are controlled by a Reb-responsive promoter. Proceedings of the National Academy of Sciences of the United States of America 98:11438−43

    doi: 10.1073/pnas.201411298

    CrossRef   Google Scholar

    [24]

    Cao R, Zhao S, Jiao G, Duan Y, Ma L, et al. 2022. OPAQUE3, encoding a transmembrane bZIP transcription factor, regulates endosperm storage protein and starch biosynthesis in rice. Plant Communications 3:100463

    doi: 10.1016/j.xplc.2022.100463

    CrossRef   Google Scholar

    [25]

    Peng B, Kong H, Li Y, Wang L, Zhong M, et al. 2014. OsAAP6 functions as an important regulator of grain protein content and nutritional quality in rice. Nature communications 5:4847

    doi: 10.1038/ncomms5847

    CrossRef   Google Scholar

    [26]

    Li Y, Fan C, Xing Y, Yun P, Luo L, et al. 2014. Chalk5 encodes a vacuolar H+-translocating pyrophosphatase influencing grain chalkiness in rice. Nature Genetics 46:398−404

    doi: 10.1038/ng.2923

    CrossRef   Google Scholar

    [27]

    Wu B, Yun P, Zhou H, Xia D, Gu Y, et al. 2022. Natural variation in WHITE-CORE RATE 1 regulates redox homeostasis in rice endosperm to affect grain quality. The Plant Cell 34:1912−32

    doi: 10.1093/plcell/koac057

    CrossRef   Google Scholar

    [28]

    Lou G, Chen P, Zhou H, Li P, Xiong J, et al. 2021. FLOURY ENDOSPERM19 encoding a class I glutamine amidotransferase affects grain quality in rice. Molecular Breeding 41:36

    doi: 10.1007/s11032-021-01226-z

    CrossRef   Google Scholar

    [29]

    Wang W, Wei X, Jiao G, Chen W, Wu Y, et al. 2020. GBSS-BINDING PROTEIN, encoding a CBM48 domain-containing protein, affects rice quality and yield. Journal of Integrative Plant Biology 62:948−66

    doi: 10.1111/jipb.12866

    CrossRef   Google Scholar

    [30]

    Zhang L, Li N, Zhang J, Zhao L, Qiu J, et al. 2022. The CBM48 domain-containing protein FLO6 regulates starch synthesis by interacting with SSIVb and GBSS in rice. Plant Molecular Biology 108:1−19

    doi: 10.1007/s11103-021-01178-0

    CrossRef   Google Scholar

    [31]

    Tian Z, Qian Q, Liu Q, Yan M, Liu X, et al. 2009. Allelic diversities in rice starch biosynthesis lead to a diverse array of rice eating and cooking qualities. Proceedings of the National Academy of Sciences of the United States of America 106:21760−65

    doi: 10.1073/pnas.0912396106

    CrossRef   Google Scholar

    [32]

    Tan YF, Sun M, Xing YZ, Hua JP, Sun XL, et al. 2001. Mapping quantitative trait loci for milling quality, protein content and color characteristics of rice using a recombinant inbred line population derived from an elite rice hybrid. Theoretical and Applied Genetics 103:1037−45

    doi: 10.1007/s001220100665

    CrossRef   Google Scholar

    [33]

    Chen P, Shen Z, Ming L, Li Y, Dan W, et al. 2018. Genetic basis of variation in rice seed storage protein (Albumin, Globulin, Prolamin, and Glutelin) content revealed by genome-wide association analysis. Frontiers in Plant Science 9:612

    doi: 10.3389/fpls.2018.00612

    CrossRef   Google Scholar

    [34]

    Xia D, Zhou H, Wang Y, Ao Y, Li Y, et al. 2022. qFC6, a major gene for crude fat content and quality in rice. Theoretical and Applied Genetics 135:2675−85

    doi: 10.1007/s00122-022-04141-9

    CrossRef   Google Scholar

    [35]

    Xia D, Wang Y, Shi Q, Wu B, Yu X, et al. 2022. Effects of Wx genotype, nitrogen fertilization, and temperature on rice grain quality. Frontiers in Plant Science 13:901541

    doi: 10.3389/fpls.2022.901541

    CrossRef   Google Scholar

    [36]

    Qiu X, Yang J, Zhang F, Niu Y, Zhao X, et al. 2021. Genetic dissection of rice appearance quality and cooked rice elongation by genome-wide association study. The Crop Journal 9:1470−80

    doi: 10.1016/j.cj.2020.12.010

    CrossRef   Google Scholar

    [37]

    Deng Z, Liu Y, Gong C, Chen B, Wang T. 2022. Waxy is an important factor for grain fissure resistance and head rice yield as revealed by a genome-wide association study. Journal of Experimental Botany 73:6942−54

    doi: 10.1093/jxb/erac330

    CrossRef   Google Scholar

    [38]

    Mandal S, Mandal RK. 2000. Seed storage proteins and approaches for improvement of their nutritional quality by genetic engineering. Current Science 79:576−89

    Google Scholar

    [39]

    Zhao L, Pan T, Cai C, Wang J, Wei C. 2016. Application of whole sections of mature cereal seeds to visualize the morphology of endosperm cell and starch and the distribution of storage protein. Journal of Cereal Science 71:19−27

    doi: 10.1016/j.jcs.2016.07.010

    CrossRef   Google Scholar

    [40]

    Long X, Guan C, Wang L, Jia L, Fu X, et al. 2023. Rice Storage Proteins: Focus on Composition, Distribution, Genetic Improvement and Effects on Rice Quality. Rice Science 30:207−21

    doi: 10.1016/j.rsci.2023.03.005

    CrossRef   Google Scholar

    [41]

    Kubota M, Saito Y, Masumura T, Kumagai T, Watanabe R, et al. 2010. Improvement in the in vivo digestibility of rice protein by alkali extraction is due to structural changes in prolamin/protein body-I particle. Bioscience, Biotechnology, and Biochemistry 74:614−19

    doi: 10.1271/bbb.90827

    CrossRef   Google Scholar

    [42]

    Tanaka K, Sugimoto T, Ogawa M, Kasai Z. 1980. Isolation and characterization of two types of protein bodies in the rice endosperm. Agricultural and Biological Chemistry 44:1633−39

    doi: 10.1080/00021369.1980.10864167

    CrossRef   Google Scholar

    [43]

    Amagliani L, O’Regan J, Kelly AL, O'Mahony J. 2017. The composition, extraction, functionality and applications of rice proteins: A review. Trends in Food Science & Technology 64:1−12

    doi: 10.1016/j.jpgs.2017.01.008

    CrossRef   Google Scholar

    [44]

    He W, Wang L, Lin Q, Yu F. 2021. Rice seed storage proteins: Biosynthetic pathways and the effects of environmental factors. Journal of Integrative Plant Biology 63:1999−2019

    doi: 10.1111/jipb.13176

    CrossRef   Google Scholar

    [45]

    Singh V, Okadome H, Toyoshima H, Isobe S, Ohtsubo K. 2000. Thermal and physicochemical properties of rice grain, flour and starch. Journal of Agricultural and Food Chemistry 48:2639−47

    doi: 10.1021/jf990374f

    CrossRef   Google Scholar

    [46]

    Martin M, Fitzgerald MA. 2002. Proteins in rice grains influence cooking properties! Journal of Cereal Science 36:285−94

    doi: 10.1006/jcrs.2001.0465

    CrossRef   Google Scholar

    [47]

    Hamaker B, Griffin VK. 1990. Changing the viscoelastic properties of cooked rice through protein disruption. Cereal Chemistry 67:261−64

    Google Scholar

    [48]

    Hamaker BR, Griffin VK. 1993. Effect of disulfide bond-containing protein on rice starch gelatinization and pasting. Cereal Chemistry 70:377−80

    Google Scholar

    [49]

    Xie L, Chen N, Duan B, Zhu Z, Liao X. 2008. Impact of proteins on pasting and cooking properties of waxy and non-waxy rice. Journal of Cereal Science 47:372−79

    doi: 10.1016/j.jcs.2007.05.018

    CrossRef   Google Scholar

    [50]

    Chávez-Murillo CE, Wang YJ, Quintero-Gutierrez AG, Bello-Pérez LA. 2011. Physicochemical, Textural, and Nutritional Characterization of Mexican Rice Cultivars. Cereal Chemistry 88:245−52

    doi: 10.1094/CCHEM-10-10-0146

    CrossRef   Google Scholar

    [51]

    Baxter G, Blanchard C, Zhao J. 2014. Effects of glutelin and globulin on the physicochemical properties of rice starch and flour. Journal of Cereal Science 60:414−20

    doi: 10.1016/j.jcs.2014.05.002

    CrossRef   Google Scholar

    [52]

    Baxter G, Blanchard C, Zhao J. 2004. Effects of prolamin on the textural and pasting properties of rice flour and starch. Journal of Cereal Science 40:205−11

    doi: 10.1016/j.jcs.2004.07.004

    CrossRef   Google Scholar

    [53]

    Zhou Z, Robards K, Helliwell S, Blanchard C. 2010. Effect of storage temperature on rice thermal properties. Food Research International 43:709−15

    doi: 10.1016/j.foodres.2009.11.002

    CrossRef   Google Scholar

    [54]

    Zhang YJ, Chen YY, Yan GJ, Du B, Zhou YR, et al. 2009. Effects of Nitrogen Nutrition on Grain Quality in Upland Rice Zhonghan 3 and Paddy Rice Yangjing 9538 Under Different Cultivation Methods. Acta Agronomica Sinica 35:1866−74

    doi: 10.1016/S1875-2780(08)60112-1

    CrossRef   Google Scholar

    [55]

    Champagne ET, Bett-Garber KL, Thomson JL, Fitzgerald MA. 2009. Unraveling the impact of nitrogen nutrition on cooked rice flavor and texture. Cereal Chemistry 86:274−80

    doi: 10.1094/cchem-86-3-0274

    CrossRef   Google Scholar

    [56]

    Okadome H. 2005. Application of Instrument-Based Multiple Texture Measurement of Cooked Milled-Rice Grains to Rice Quality Evaluation. Japan Agricultural Research Quarterly 39:261−68

    doi: 10.6090/jarq.39.261

    CrossRef   Google Scholar

    [57]

    Yang Y, Shen Z, Li Y, Xu C, Xia H, et al. 2022. Rapid improvement of rice eating and cooking quality through gene editing toward glutelin as target. Journal of Integrative Plant Biology 64:1860−65

    doi: 10.1111/jipb.13334

    CrossRef   Google Scholar

    [58]

    Ohtsubo K, Nakamura S. 2017. Evaluation of Palatability of Cooked Rice. In Advances in International Rice Research, ed. Li J. Rijeka: IntechOpen. https://doi.org/10.5772/66398

    [59]

    Chikubu S, Watanabe S, Sugimoto T, Manabe N, Sakai F, et al. 1985. Establishment of palatability estimation formula of rice by multiple regression analysis. Journal of the Japanese Society of Starch Science 32:51−60

    doi: 10.5458/jag1972.32.51

    CrossRef   Google Scholar

    [60]

    Fitzgerald MA, McCouch SR, Hall RD. 2009. Not just a grain of rice: The quest for quality. Trends in Plant Science 14:133−39

    doi: 10.1016/j.tplants.2008.12.004

    CrossRef   Google Scholar

    [61]

    Li H, Prakash S, Nicholson TM, Fitzgerald MA, Gilbert RG. 2015. The importance of amylose and amylopectin fine structure for textural properties of cooked rice grains. Food Chemistry 196:702−11

    doi: 10.1016/j.foodchem.2015.09.112

    CrossRef   Google Scholar

    [62]

    Zhou L, Zhang C, Zhang Y, Wang C, Liu Q. 2022. Genetic manipulation of endosperm amylose for designing superior quality rice to meet the demands in the 21st century. Journal of Cereal Science 105:103481

    doi: 10.1016/j.jcs.2022.103481

    CrossRef   Google Scholar

    [63]

    Huang L, Tan H, Zhang C, Li Q, Liu Q. 2021. Starch biosynthesis in cereal endosperms: An updated review over the last decade. Plant Communications 2:100237

    doi: 10.1016/j.xplc.2021.100237

    CrossRef   Google Scholar

    [64]

    Li P, Chen YH, Lu J, Zhang CQ, Liu QQ, et al. 2022. Genes and their molecular functions determining seed structure, components, and quality of rice. Rice 15:18

    doi: 10.1186/s12284-022-00562-8

    CrossRef   Google Scholar

    [65]

    Adebowale KO, Lawal OS. 2003. Functional properties and retrogradation behaviour of native and chemically modified starch of mucuna bean (Mucuna pruriens). Journal of the Science of Food and Agriculture 83:1541−6

    doi: 10.1002/jsfa.1569

    CrossRef   Google Scholar

    [66]

    Singh J, Kaur L, McCarthy OJ. 2007. Factors influencing the physico-chemical, morphological, thermal and rheological properties of some chemically modified starches for food applications—A review. Food Hydrocolloids 21:1−22

    doi: 10.1016/j.foodhyd.2006.02.006

    CrossRef   Google Scholar

    [67]

    Wang S, Li C, Copeland L, Niu Q, Wang S. 2015. Starch Retrogradation: A Comprehensive Review. Comprehensive Reviews in Food Science and Food Safety 14:568−85

    doi: 10.1111/1541-4337.12143

    CrossRef   Google Scholar

    [68]

    Sanadya A, Yadu A, Raj J, Chandrakar H, Singh R. 2023. Effect of temperature on growth, quality, yield attributing characters and yield of rice – A review. International Journal of Environment and Climate Change 13:804−14

    doi: 10.9734/ijecc/2023/v13i82014

    CrossRef   Google Scholar

    [69]

    Tsukaguchi T, Iida Y. 2008. Effects of assimilate supply and high temperature during grain-filling period on the occurrence of various types of chalky kernels in rice plants (Oryza sativa L.). Plant Production Science 11:203−10

    doi: 10.1626/pps.11.203

    CrossRef   Google Scholar

    [70]

    Jin Z, Qian C, Yang J, Liu H, Jin X. 2005. Effect of temperature at grain filling stage on activities of key enzymes related to starch synthesis and grain quality of rice. Rice Science 12:261−66

    Google Scholar

    [71]

    Liang CG, Liu J, Wang Y, Xiong D, Ding CB, et al. 2015. Low light during grain filling stage Deteriorates rice cooking quality, but not nutritional value. Rice Science 22:197−206

    doi: 10.1016/j.rsci.2015.04.003

    CrossRef   Google Scholar

    [72]

    Goufo P, Falco V, Brites C, Wessel DF, Kratz S, et al. 2014. Effect of Elevated Carbon Dioxide Concentration on Rice Quality: Nutritive Value, Color, Milling, Cooking, and Eating Qualities. Cereal Chemistry 91:513−21

    doi: 10.1094/CCHEM-12-13-0256-R

    CrossRef   Google Scholar

    [73]

    Bloom AJ, Burger M, Rubio Asensio JS, Cousins AB. 2010. Carbon dioxide enrichment inhibits nitrate assimilation in wheat and Arabidopsis. Science 328:899−903

    doi: 10.1126/science.1186440

    CrossRef   Google Scholar

    [74]

    Lal R. 2007. Anthropogenic Influences on World Soils and Implications to Global Food Security. Advances in Agronomy 93:69−93

    doi: 10.1016/S0065-2113(06)93002-8

    CrossRef   Google Scholar

    [75]

    Dingkuhn M, Le Gal PY. 1996. Effect of drainage date on yield and dry matter partitioning in irrigated rice. Field Crops Research 46:117−26

    doi: 10.1016/0378-4290(95)00094-1

    CrossRef   Google Scholar

    [76]

    Cheng W, Zhang G, Zhao G, Yao H, Xu H. 2003. Variation in rice quality of different cultivars and grain positions as affected by water management. Field Crops Research 80:245−52

    doi: 10.1016/S0378-4290(02)00193-4

    CrossRef   Google Scholar

    [77]

    Upadhyay R, Banjara M, Thombare D, Yankanchi S, Chandel G. 2021. Deciphering the effect of different nitrogen doses on grain protein content, quality attributes and yield related traits of rice. Oryza-An International Journal on Rice 58:530−9

    doi: 10.35709/ory.2021.58.4.9

    CrossRef   Google Scholar

    [78]

    Chen Y, Wang M, Ouwerkerk PBF. 2012. Molecular and environmental factors determining grain quality in rice. Food and Energy Security 1:111−32

    doi: 10.1002/fes3.11

    CrossRef   Google Scholar

    [79]

    Bahmaniar MA, Ranjbar GA. 2007. Response of Rice (Oryza sativa L.) Cooking Quality Properties to Nitrogen and Potassium Application. Pakistan Journal of Biological Sciences 10:1880−84

    doi: 10.3923/pjbs.2007.1880.1884

    CrossRef   Google Scholar

    [80]

    Siscar-Lee JJH, Juliano BO, Qureshi RH, Akbar M. 1990. Effect of saline soil on grain quality of rices differing in salinity tolerance. Plant Foods for Human Nutrition 40:31−36

    doi: 10.1007/BF02193777

    CrossRef   Google Scholar

    [81]

    Hillerislambers D, Rutger JN, Qualset CO, Wiser WJ. 1973. Genetic and environmental variation in protein content of rice (Oryza sativa L.). Euphytica 22:264−73

    doi: 10.1007/BF00022634

    CrossRef   Google Scholar

    [82]

    Tsuzuki E, Furusho M. 1986. Studies on the Characteristics of Scented Rice: X. A trial of rice breeding for high protein variety (2). Japanese Journal of Crop Science 55:7−14

    doi: 10.1626/jcs.55.7

    CrossRef   Google Scholar

    [83]

    Yang Y, Guo M, Sun S, Zou Y, Yin S, et al. 2019. Natural variation of OsGluA2 is involved in grain protein content regulation in rice. Nature Communications 10:1949

    doi: 10.1038/s41467-019-09919-y

    CrossRef   Google Scholar

    [84]

    Liu Z, Cheng F, Zhang G. 2005. Grain phytic acid content in japonica rice as affected by cultivar and environment and its relation to protein content. Food Chemistry 89:49−52

    doi: 10.1016/j.foodchem.2004.01.081

    CrossRef   Google Scholar

    [85]

    Webb BD, Bollich CN, Adair CR, Johnston TH. 1968. Characteristics of rice varieties in the U.S. department of agriculture collection. Crop Science 8:361−65

    doi: 10.2135/cropsci1968.0011183x000800030029x

    CrossRef   Google Scholar

    [86]

    Aluko G, Martinez C, Tohme J, Castano Rodriguez C, Bergman C, et al. 2004. QTL mapping of grain quality traits from the interspecific cross Oryza sativa × O. glaberrima. Theoretical and Applied Genetics 109:630−39

    doi: 10.1007/s00122-004-1668-y

    CrossRef   Google Scholar

    [87]

    Hu ZL, Li P, Zhou MQ, Zhang Z, Wang LX, et al. 2004. Mapping of quantitative trait loci (QTLs) for rice protein and fat content using doubled haploid lines. Euphytica 135:47−54

    doi: 10.1023/B:EUPH.0000009539.38916.32

    CrossRef   Google Scholar

    [88]

    Kepiro JL, McClung AM, Chen MH, Yeater K, Fjellstrom RG. 2008. Mapping QTLs for milling yield and grain characteristics in a tropical japonica long grain cross. Journal of Cereal Science 48:477−85

    doi: 10.1016/j.jcs.2007.12.001

    CrossRef   Google Scholar

    [89]

    Wang L, Zhong M, Li X, Yuan D, Xu Y, et al. 2008. The QTL controlling amino acid content in grains of rice (Oryza sativa) are co-localized with the regions involved in the amino acid metabolism pathway. Molecular Breeding 21:127−37

    doi: 10.1007/s11032-007-9141-7

    CrossRef   Google Scholar

    [90]

    Lou J, Chen L, Yue G, Lou Q, Mei H, et al. 2009. QTL mapping of grain quality traits in rice. Journal of Cereal Science 50:145−51

    doi: 10.1016/j.jcs.2009.04.005

    CrossRef   Google Scholar

    [91]

    Ye G, Liang S, Wan J. 2010. QTL mapping of protein content in rice using single chromosome segment substitution lines. Theoretical and Applied Genetics 121:741−50

    doi: 10.1007/s00122-010-1345-2

    CrossRef   Google Scholar

    [92]

    Liu X, Wan X, Ma X, Wan J. 2010. Dissecting the genetic basis for the effect of rice chalkiness, amylose content, protein content, and rapid viscosity analyzer profile characteristics on the eating quality of cooked rice using the chromosome segment substitution line population across eight environments. Genome 54:64−80

    doi: 10.1139/G10-070

    CrossRef   Google Scholar

    [93]

    Bruno E, Choi YS, Chung IK, Kim KM. 2017. QTLs and analysis of the candidate gene for amylose, protein, and moisture content in rice (Oryza sativa L.). 3 Biotech 7:40

    doi: 10.1007/s13205-017-0687-8

    CrossRef   Google Scholar

    [94]

    Kashiwagi T, Munakata J. 2018. Identification and characteristics of quantitative trait locus for grain protein content, TGP12, in rice (Oryza sativa L.). Euphytica 214:165

    doi: 10.1007/s10681-018-2249-5

    CrossRef   Google Scholar

    [95]

    Park SG, Park HS, Baek MK, Jeong JM, Cho YC, et al. 2019. Improving the glossiness of cooked rice, an important component of visual rice grain quality. Rice 12:87

    doi: 10.1186/s12284-019-0348-0

    CrossRef   Google Scholar

    [96]

    Zhang W, Bi J, Chen L, Zheng L, Ji S, et al. 2008. QTL mapping for crude protein and protein fraction contents in rice (Oryza sativa L.). Journal of Cereal Science 48:539−47

    doi: 10.1016/j.jcs.2007.11.010

    CrossRef   Google Scholar

    [97]

    Yu YH, Li G, Fan Y, Zhang KQ, Min J, et al. 2009. Genetic relationship between grain yield and the contents of protein and fat in a recombinant inbred population of rice. Journal of Cereal Science 50:121−25

    doi: 10.1016/j.jcs.2009.03.008

    CrossRef   Google Scholar

    [98]

    Zheng L, Zhang W, Chen X, Ma J, Chen W, et al. 2011. Dynamic QTL Analysis of Rice Protein Content and Protein Index Using Recombinant Inbred Lines. Journal of Plant Biology 54:321−28

    doi: 10.1007/s12374-011-9170-y

    CrossRef   Google Scholar

    [99]

    Cruz M, Arbelaez J, Loaiza K, Cuasquer J, Rosas J, et al. 2021. Genetic and phenotypic characterization of rice grain quality traits to define research strategies for improving rice milling, appearance, and cooking qualities in Latin America and the Caribbean. The Plant Genome 14:e20134

    doi: 10.1002/tpg2.20134

    CrossRef   Google Scholar

    [100]

    Hickey LT, Hafeez AN, Robinson H, Jackson SA, Leal-Bertioli SCM, et al. 2019. Breeding crops to feed 10 billion. Nature Biotechnology 37:744−54

    doi: 10.1038/s41587-019-0152-9

    CrossRef   Google Scholar

    [101]

    Crossa J, Pérez-Rodríguez P, Cuevas J, Montesinos-López O, Jarquín D, et al. 2017. Genomic selection in plant breeding: Methods, models, and perspectives. Trends in Plant Science 22:961−75

    doi: 10.1016/j.tplants.2017.08.011

    CrossRef   Google Scholar

    [102]

    Chen W, Gao Y, Xie W, Gong L, Lu K, et al. 2014. Genome-wide association analyses provide genetic and biochemical insights into natural variation in rice metabolism. Nature Communications 46:714−21

    doi: 10.1038/ng.3007

    CrossRef   Google Scholar

    [103]

    Chen P, Lou G, Wang Y, Chen J, Chen W, et al. 2022. The genetic basis of grain protein content in rice by genome-wide association analysis. Molecular Breeding 43:1

    doi: 10.1007/s11032-022-01347-z

    CrossRef   Google Scholar

    [104]

    Huang X, Zhao Y, Wei X, Li C, Wang A, et al. 2011. Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nature Genetics 44:32−39

    doi: 10.1038/ng.1018

    CrossRef   Google Scholar

    [105]

    Verma RK, Chetia SK, Sharma V, Baishya S, Sharma H, et al. 2022. GWAS to spot candidate genes associated with grain quality traits in diverse rice accessions of North East India. Molecular Biology Reports 49:5365−77

    doi: 10.1007/s11033-021-07113-2

    CrossRef   Google Scholar

    [106]

    Wang X, Pang Y, Zhang J, Wu Z, Chen K, et al. 2017. Genome-wide and gene-based association mapping for rice eating and cooking characteristics and protein content. Scientific Reports 7:17203

    doi: 10.1038/s41598-017-17347-5

    CrossRef   Google Scholar

    [107]

    Zhang Y, Zhang S, Zhang J, Wei W, Zhu T, et al. 2023. Improving rice eating and cooking quality by enhancing endogenous expression of a nitrogen-dependent floral regulator. Plant Biotechnology Journal

    doi: 10.1111/pbi.14160

    CrossRef   Google Scholar

    [108]

    Li S, Tian Y, Wu K, Ye Y, Yu J, et al. 2018. Modulating plant growth-metabolism coordination for sustainable agriculture. Nature 560:595−600

    doi: 10.1038/s41586-018-0415-5

    CrossRef   Google Scholar

    [109]

    Fang L, Ma L, Zhao S, Cao R, Jiao G, et al. 2022. Alanine aminotransferase (OsAlaAT1) modulates nitrogen utilization, grain yield and quality in rice. Journal of Genetics and Genomics 49:510−13

    doi: 10.1016/j.jgg.2022.02.028

    CrossRef   Google Scholar

    [110]

    Huang Y, Wang H, Zhu Y, Huang X, Li S, et al. 2022. THP9 enhances seed protein content and nitrogen-use efficiency in maize. Nature 612:292−300

    doi: 10.1038/s41586-022-05441-2

    CrossRef   Google Scholar

    [111]

    Wei S, Li X, Lu Z, Zhang H, Ye X, et al. 2022. A transcriptional regulator that boosts grain yields and shortens the growth duration of rice. Science 377:eabi8455

    doi: 10.1126/science.abi8455

    CrossRef   Google Scholar

    [112]

    McKenzie KS, Rutger JN. 1983. Genetic Analysis of Amylose Content, Alkali Spreading Score, and Grain Dimensions in Rice. Crop Science 23:306−13

    doi: 10.2135/cropsci1983.0011183x002300020031x

    CrossRef   Google Scholar

    [113]

    Schaeffer GW, Sharpe FT. 1990. Modification of amino acid composition of endosperm proteins from in-vitro-selected high lysine mutants in rice. Theoretical and Applied Genetics 80:841−46

    doi: 10.1007/BF00224202

    CrossRef   Google Scholar

    [114]

    Schaeffer GW, Sharpe FT. 1987. Increased Lysine and Seed Storage Protein in Rice Plants Recovered from Calli Selected with Inhibitory Levels of Lysine plus Threonine and S-(2-Aminoethyl)cysteine. Plant Physiology 84:509−15

    doi: 10.1104/pp.84.2.509

    CrossRef   Google Scholar

    [115]

    Juliano BO, Antonio AA, Esmama BV. 1973. Effects of Protein Content on the Distribution and Properties of Rice Protein. Journal of the Science of Food and Agriculture 24:295−306

    doi: 10.1002/jsfa.2740240306

    CrossRef   Google Scholar

    [116]

    Mochizuki T, Hara S. 2000. Usefulness of the low protein rice on the diet therapy in patients with chronic renal failure. Nihon Jinzo Gakkai shi 42:24−29(In Japanese

    Google Scholar

    [117]

    Zhang Y, Zhang S, Zhou J, Lin J, Wang Y, et al. 2015. Enhancement and identification of new rice germplasms with low glutelin content. Journal of Plant Genetic Resources 16:158−62

    doi: 10.13430/j.cnki.jpgr.2015.01.024

    CrossRef   Google Scholar

    [118]

    Lee SI, Kim HU, Lee YH, Suh SC, Lim YP, et al. 2001. Constitutive and seed-specific expression of a maize lysine-feedback-insensitive dihydrodipicolinate synthase gene leads to increased free lysine levels in rice seeds. Molecular Breeding 8:75−84

    doi: 10.1023/A:1011977219926

    CrossRef   Google Scholar

    [119]

    Liu X, Zhang C, Wang X, Liu Q, Yuan D, et al. 2016. Development of high-lysine rice via endosperm-specific expression of a foreign LYSINE RICH PROTEIN gene. BMC Plant Biology 16:147

    doi: 10.1186/s12870-016-0837-x

    CrossRef   Google Scholar

    [120]

    Lee TTT, Wang MMC, Hou RCW, Chen LJ, Su RC, et al. 2003. Enhanced Methionine and Cysteine Levels in Transgenic Rice Seeds by the Accumulation of Sesame 2S Albumin. Bioscience, Biotechnology, and Biochemistry 67:1699−705

    doi: 10.1271/bbb.67.1699

    CrossRef   Google Scholar

    [121]

    Hagan ND, Upadhyaya N, Tabe LM, Higgins TJV. 2003. The redistribution of protein sulfur in transgenic rice expressing a gene for a foreign, sulfur-rich protein. The Plant Journal 34:1−11

    doi: 10.1046/j.1365-313X.2003.01699.x

    CrossRef   Google Scholar

    [122]

    Zhou Y, Cai H, Xiao J, Li X, Zhang Q, Lian X. 2009. Over-expression of aspartate aminotransferase genes in rice resulted in altered nitrogen metabolism and increased amino acid content in seeds. Theoretical and Applied Genetics 118:1381−90

    doi: 10.1007/s00122-009-0988-3

    CrossRef   Google Scholar

    [123]

    Wakasa K, Hasegawa H, Nemoto H, Matsuda F, Miyazawa H, et al. 2006. High-level tryptophan accumulation in seeds of transgenic rice and its limited effects on agronomic traits and seed metabolite profile. Journal of Experimental Botany 57:3069−78

    doi: 10.1093/jxb/erl068

    CrossRef   Google Scholar

    [124]

    Bashirullah A, Cooperstock RL, Lipshitz HD. 2001. Spatial and temporal control of RNA stability. Proceedings of the National Academy of Sciences of the United States of America 98:7025−28

    doi: 10.1073/pnas.111145698

    CrossRef   Google Scholar

    [125]

    Hollams EM, Giles KM, Thomson AM, Leedman PJ. 2002. mRNA stability and the control of gene expression: Implications for human disease. Neurochemical Research 27:957−80

    doi: 10.1023/A:1020992418511

    CrossRef   Google Scholar

    [126]

    Merritt C, Rasoloson D, Ko D, Seydoux G. 2008. 3′ UTRs are the primary regulators of gene expression in the C. elegans germline. Current Biology 18:1476−82

    doi: 10.1016/j.cub.2008.08.013

    CrossRef   Google Scholar

    [127]

    Li WJ, Dai LL, Chai ZJ, Yin ZJ, Qu LQ. 2012. Evaluation of seed storage protein gene 3′-untranslated regions in enhancing gene expression in transgenic rice seed. Transgenic Research 21:545−53

    doi: 10.1007/s11248-011-9552-4

    CrossRef   Google Scholar

    [128]

    Yang L, Wakasa Y, Kawakatsu T, Takaiwa F. 2009. The 3′-untranslated region of rice glutelin GluB-1 affects accumulation of heterologous protein in transgenic rice. Biotechnology Letters 31:1625−31

    doi: 10.1007/s10529-009-0056-8

    CrossRef   Google Scholar

    [129]

    Chen Z, Du H, Tao Y, Xu Y, Wang F, et al. 2022. Efficient breeding of low glutelin content rice germplasm by simultaneous editing multiple glutelin genes via CRISPR/Cas9. Plant Science 324:111449

    doi: 10.1016/j.plantsci.2022.111449

    CrossRef   Google Scholar

    [130]

    Kang HG, Park S, Matsuoka M, An G. 2005. White-core endosperm floury endosperm-4 in rice is generated by knockout mutations in the C4-type pyruvate orthophosphate dikinase gene (OsPPDKB). The Plant journal 42:901−11

    doi: 10.1111/j.1365-313X.2005.02423.x

    CrossRef   Google Scholar

    [131]

    Long W, Dong B, Wang Y, Pan P, Wang Y, et al. 2017. FLOURY ENDOSPERM8, encoding the UDP-glucose pyrophosphorylase 1, affects the synthesis and structure of starch in rice endosperm. Journal of Plant Biology 60:513−22

    doi: 10.1007/s12374-017-0066-3

    CrossRef   Google Scholar

    [132]

    Yang J, Kim SR, Lee SK, Choi H, Jeon JS, et al. 2015. Alanine aminotransferase 1 (OsAlaAT1) plays an essential role in the regulation of starch storage in rice endosperm. Plant Science 240:79−89

    doi: 10.1016/j.plantsci.2015.07.027

    CrossRef   Google Scholar

    [133]

    Zhong M, Liu X, Liu F, Ren Y, Wang Y, et al. 2019. FLOURY ENDOSPERM12 encoding alanine aminotransferase 1 regulates carbon and nitrogen metabolism in rice. Journal of Plant Biology 62:61−73

    doi: 10.1007/s12374-018-0288-z

    CrossRef   Google Scholar

    [134]

    You X, Zhang W, Hu J, Jing R, Cai Y, et al. 2019. FLOURY ENDOSPERM15 encodes a glyoxalase I involved in compound granule formation and starch synthesis in rice endosperm. Plant Cell Reports 38:345−59

    doi: 10.1007/s00299-019-02370-9

    CrossRef   Google Scholar

    [135]

    Teng X, Zhong M, Zhu X, Wang C, Ren Y, et al. 2019. FLOURY ENDOSPERM16 encoding a NAD-dependent cytosolic malate dehydrogenase plays an important role in starch synthesis and seed development in rice. Plant Biotechnology Journal 17:1914−27

    doi: 10.1111/pbi.13108

    CrossRef   Google Scholar

    [136]

    Long W, Wang Y, Zhu S, Jing W, Wang Y, et al. 2018. FLOURY SHRUNKEN ENDOSPERM1 connects phospholipid metabolism and amyloplast development in rice. Plant Physiology 177:698−712

    doi: 10.1104/pp.17.01826

    CrossRef   Google Scholar

    [137]

    Tang XJ, Peng C, Zhang J, Cai Y, You XM, et al. 2016. ADP-glucose pyrophosphorylase large subunit 2 is essential for storage substance accumulation and subunit interactions in rice endosperm. Plant Science 249:70−83

    doi: 10.1016/j.plantsci.2016.05.010

    CrossRef   Google Scholar

    [138]

    Chen Y, Luo L, Xu F, Xu X, Bao J. 2022. Carbohydrate repartitioning in the riceStarch Branching Enzyme IIb mutant stimulates higher resistant starch content and lower seed weight revealed by multiomics analysis. Journal of Agricultural and Food Chemistry 70:9802−16

    doi: 10.1021/acs.jafc.2c03737

    CrossRef   Google Scholar

    [139]

    Satoh H, Shibahara K, Tokunaga T, Nishi A, Tasaki M, et al. 2008. Mutation of the plastidial α-Glucan phosphorylase gene in rice affects the synthesis and structure of starch in the endosperm. The Plant Cell 20:1833−49

    doi: 10.1105/tpc.107.054007

    CrossRef   Google Scholar

    [140]

    Yang H, Liu L, Wu K, Liu S, Liu X, et al. 2021. FLOURY AND SHRUNKEN ENDOSPERM6 encodes a glycosyltransferase and is essential for the development of rice endosperm. Journal of Plant Biology 65:187−98

    doi: 10.1007/s12374-020-09293-z

    CrossRef   Google Scholar

    [141]

    Cai Y, Li S, Jiao G, Sheng Z, Wu Y, et al. 2018. OsPK2 encodes a plastidic pyruvate kinase involved in rice endosperm starch synthesis, compound granule formation and grain filling. Plant Biotechnology Journal 16:1878−91

    doi: 10.1111/pbi.12923

    CrossRef   Google Scholar

    [142]

    Wang E, Wang J, Zhu X, Hao W, Wang L, et al. 2008. Control of rice grain-filling and yield by a gene with potential signature of domestication. Nature Genetics 40:1370−74

    doi: 10.1038/ng.220

    CrossRef   Google Scholar

    [143]

    Han X, Wang Y, Liu X, Jiang L, Ren Y, et al. 2012. The failure to express a protein disulphide isomerase-like protein results in a floury endosperm and an endoplasmic reticulum stress response in rice. Journal of Experimental Botany 63:121−30

    doi: 10.1093/jxb/err262

    CrossRef   Google Scholar

    [144]

    Matsushima R, Maekawa M, Kusano M, Tomita K, Kondo H, et al. 2016. Amyloplast membrane protein SUBSTANDARD STARCH GRAIN6 controls starch grain size in rice endosperm. Plant Physiology 170:1445−59

    doi: 10.1104/pp.15.01811

    CrossRef   Google Scholar

    [145]

    Duan E, Wang Y, Liu L, Zhu J, Zhong M, et al. 2016. Pyrophosphate: fructose-6-phosphate 1-phosphotransferase (PFP) regulates carbon metabolism during grain filling in rice. Plant Cell Reports 35:1321−31

    doi: 10.1007/s00299-016-1964-4

    CrossRef   Google Scholar

    [146]

    Lei J, Teng X, Wang Y, Jiang X, Zhao H, et al. 2022. Plastidic pyruvate dehydrogenase complex E1 component subunit alpha1 is involved in galactolipid biosynthesis required for amyloplast development in rice. Plant Biotechnology Journal 20:437−53

    doi: 10.1111/pbi.13727

    CrossRef   Google Scholar

    [147]

    Chen X, Ji Y, Zhao W, Niu H, Yang X, et al. 2023. Fructose-6-phosphate-2-kinase/Fructose-2, 6-bisphosphatase Regulates Energy Metabolism and Synthesis of Storage Products in Developing Rice Endosperm. Plant Science 326:111503

    doi: 10.1016/j.plantsci.2022.111503

    CrossRef   Google Scholar

    [148]

    Hwang SK, Koper K, Satoh H, Okita TW. 2016. Rice endosperm starch phosphorylase (Pho1) assembles with disproportionating enzyme (Dpe1) to form a protein complex that enhances synthesis of malto-oligosaccharides. Journal of Biological Chemistry 291:19994−20007

    doi: 10.1074/jbc.M116.735449

    CrossRef   Google Scholar

    [149]

    Xiong Y, Ren Y, Li W, Wu F, Yang W, et al. 2019. NF-YC12 is a key multi-functional regulator of accumulation of seed storage substances in rice. Journal of Experimental Botany 70:3765−80

    doi: 10.1093/jxb/erz168

    CrossRef   Google Scholar

    [150]

    Kawakatsu T, Yamamoto MP, Touno SM, Yasuda H, Takaiwa F. 2009. Compensation and interaction between RISBZ1 and RPBF during grain filling in rice. The Plant journal 59:908−20

    doi: 10.1111/j.1365-313X.2009.03925.x

    CrossRef   Google Scholar

    [151]

    Nakase M, Aoki N, Matsuda T, Adachi T. 1997. Characterization of a novel rice bZIP protein which binds to the α-globulin promoter. Plant Molecular Biology 33:513−22

    doi: 10.1023/A:1005784717782

    CrossRef   Google Scholar

    [152]

    Wu MW, Liu J, Bai X, Chen WQ, Ren Y, et al. 2023. Transcription factors NAC20 and NAC26 interact with RPBF to activate albumin accumulations in rice endosperm. Plant Biotechnology Journal 21:890−92

    doi: 10.1111/pbi.13994

    CrossRef   Google Scholar

    [153]

    She KC, Kusano H, Koizumi K, Yamakawa H, Hakata M, et al. 2010. A novel factor FLOURY ENDOSPERM2 is involved in regulation of rice grain size and starch quality. The Plant Cell 22:3280−94

    doi: 10.1105/tpc.109.070821

    CrossRef   Google Scholar

    [154]

    Peng C, Wang Y, Liu F, Ren Y, Zhou K, et al. 2014. FLOURY ENDOSPERM6 encodes a CBM48 domain-containing protein involved in compound granule formation and starch synthesis in rice endosperm. The Plant Journal 77:917−30

    doi: 10.1111/tpj.12444

    CrossRef   Google Scholar

    [155]

    Zhang L, Ren Y, Lu B, Yang C, Feng Z, et al. 2016. FLOURY ENDOSPERM7 encodes a regulator of starch synthesis and amyloplast development essential for peripheral endosperm development in rice. Journal of Experimental Botany 67:633−47

    doi: 10.1093/jxb/erv469

    CrossRef   Google Scholar

    [156]

    Tabassum R, Dosaka T, Ichida H, Morita R, Ding Y, et al. 2020. FLOURY ENDOSPERM11-2 encodes plastid HSP70-2 involved with the temperature-dependent chalkiness of rice (Oryza sativa L.) grains. The Plant Journal 103:604−16

    doi: 10.1111/tpj.14752

    CrossRef   Google Scholar

    [157]

    Fu FF, Xue HW. 2010. Coexpression analysis identifies rice starch regulator1, a rice AP2/EREBP family transcription factor, as a novel rice starch biosynthesis regulator. Plant Physiology 154:927−38

    doi: 10.1104/pp.110.159517

    CrossRef   Google Scholar

    [158]

    Li Z, Wei X, Tong X, Zhao J, Liu X, et al. 2022. The OsNAC23-Tre6P-SnRK1a feed-forward loop regulates sugar homeostasis and grain yield in rice. Molecular Plant 15:706−22

    doi: 10.1016/j.molp.2022.01.016

    CrossRef   Google Scholar

    [159]

    Ren Y, Huang Z, Jiang H, Wang Z, Wu F, et al. 2021. A heat stress responsive NAC transcription factor heterodimer plays key roles in rice grain filling. Journal of Experimental Botany 72:2947−64

    doi: 10.1093/jxb/erab027

    CrossRef   Google Scholar

    [160]

    Jin SK, Zhang MQ, Leng YJ, Xu LN, Jia SW, et al. 2022. OsNAC129 regulates seed development and plant growth and participates in the brassinosteroid signaling pathway. Frontiers in Plant Science 13:905148

    doi: 10.3389/fpls.2022.905148

    CrossRef   Google Scholar

    [161]

    Yu X, Xia S, Xu Q, Cui Y, Gong M, et al. 2020. ABNORMAL FLOWER AND GRAIN 1 encodes OsMADS6 and determines palea identity and affects rice grain yield and quality. Science China Life Sciences 63:228−38

    doi: 10.1007/s11427-019-1593-0

    CrossRef   Google Scholar

    [162]

    Yang X, Wu F, Lin X, Du X, Chong K, et al. 2012. Live and Let Die - The Bsister MADS-Box gene OsMADS29 controls the degeneration of cells in maternal tissues during seed development of rice (Oryza sativa). PLoS One 7:e51435

    doi: 10.1371/journal.pone.0051435

    CrossRef   Google Scholar

    [163]

    Liu J, Wu X, Yao X, Yu R, Larkin P, Liu C-M. 2018. Mutations in the DNA demethylase OsROS1 result in a thickened aleurone and improved nutritional value in rice grains. Proceedings of the National Academy of Sciences of the United States of America 115:201806304

    doi: 10.1073/pnas.1806304115

    CrossRef   Google Scholar

    [164]

    Yan M, Pan T, Zhu Y, Jiang X, Yu M, et al. 2022. FLOURY ENDOSPERM20 encoding SHMT4 is required for rice endosperm development. Plant Biotechnology Journal 20:1438−40

    doi: 10.1111/pbi.13858

    CrossRef   Google Scholar

    [165]

    Wu M, Ren Y, Cai M, Wang Y, Zhu S, et al. 2019. Rice FLOURY ENDOSPERM10 encodes a pentatricopeptide repeat protein that is essential for the trans-splicing of mitochondrial nad1 intron 1 and endosperm development. New Phytologist 223:736−50

    doi: 10.1111/nph.15814

    CrossRef   Google Scholar

    [166]

    Xue M, Liu L, Yu Y, Zhu J, Gao H, et al. 2019. Lose-of-function of a rice nucleolus-localized pentatricopeptide repeat protein is responsible for the floury endosperm14 mutant phenotypes. Rice 12:100

    doi: 10.1186/s12284-019-0359-x

    CrossRef   Google Scholar

    [167]

    Yu M, Wu M, Ren Y, Wang Y, Li J, et al. 2021. Rice FLOURY ENDOSPERM 18 encodes a pentatricopeptide repeat protein required for 5′ processing of mitochondrial nad5 mRNA and endosperm development. Journal of Integrative Plant Biology 63:834−47

    doi: 10.1111/jipb.13049

    CrossRef   Google Scholar

    [168]

    Kim SR, Yang JI, Moon S, Ryu CH, An K, et al. 2009. Rice OGR1 encodes a pentatricopeptide repeat–DYW protein and is essential for RNA editing in mitochondria. The Plant Journal 59:738−49

    doi: 10.1111/j.1365-313X.2009.03909.x

    CrossRef   Google Scholar

    [169]

    Hao Y, Wang Y, Wu M, Zhu X, Teng X, et al. 2019. The nucleus-localized PPR protein OsNPPR1 is important for mitochondrial function and endosperm development in rice. Journal of Experimental Botany 70:4705−20

    doi: 10.1093/jxb/erz226

    CrossRef   Google Scholar

    [170]

    Yang H, Wang Y, Tian Y, Teng X, Lv Z, et al. 2022. Rice FLOURY ENDOSPERM22, encoding a pentatricopeptide repeat protein, is involved in both mitochondrial RNA splicing and editing and is crucial for endosperm development. Journal of Integrative Plant Biology 65:755−71

    doi: 10.1111/jipb.13402

    CrossRef   Google Scholar

    [171]

    Wang R, Ren Y, Yan H, Teng X, Zhu X, et al. 2021. ENLARGED STARCH GRAIN1 affects amyloplast development and starch biosynthesis in rice endosperm. Plant Science 305:110831

    doi: 10.1016/j.plantsci.2021.110831

    CrossRef   Google Scholar

    [172]

    Li S, Wei X, Ren Y, Qiu J, Jiao G, et al. 2017. OsBT1 encodes an ADP-glucose transporter involved in starch synthesis and compound granule formation in rice endosperm. Scientific Reports 7:40124

    doi: 10.1038/srep40124

    CrossRef   Google Scholar

    [173]

    Wakasa Y, Yasuda H, Oono Y, Kawakatsu T, Hirose S, et al. 2011. Expression of ER quality control-related genes in response to changes in BiP1 levels in developing rice endosperm. The Plant Journal 65:675−89

    doi: 10.1111/j.1365-313X.2010.04453.x

    CrossRef   Google Scholar

    [174]

    Wang X, Zhou W, Lu Z, Ouyang Y, Chol Su O, et al. 2015. A lipid transfer protein, OsLTPL36, is essential for seed development and seed quality in rice. Plant Science 239:200−8

    doi: 10.1016/j.plantsci.2015.07.016

    CrossRef   Google Scholar

    [175]

    Wang Y, Ren Y, Liu X, Jiang L, Chen L, et al. 2010. OsRab5a regulates endomembrane organization and storage protein trafficking in rice endosperm cells. The Plant Journal 64:812−24

    doi: 10.1111/j.1365-313X.2010.04370.x

    CrossRef   Google Scholar

    [176]

    Tian L, Dai LL, Yin ZJ, Fukuda M, Kumamaru T, et al. 2013. Small GTPase Sar1 is crucial for proglutelin and α-globulin export from the endoplasmic reticulum in rice endosperm. Journal of Experimental Botany 64:2831−45

    doi: 10.1093/jxb/ert128

    CrossRef   Google Scholar

    [177]

    Ren Y, Wang Y, Liu F, Zhou K, Ding Y, et al. 2014. GLUTELIN PRECURSOR ACCUMULATION3 encodes a regulator of post-golgi vesicular traffic essential for vacuolar protein sorting in rice endosperm. The Plant Cell 26:410−25

    doi: 10.1105/tpc.113.121376

    CrossRef   Google Scholar

    [178]

    Wang Y, Liu F, Ren Y, Wang Y, Liu X, et al. 2016. GOLGI TRANSPORT 1B regulates protein export from endoplasmic reticulum in rice endosperm cells. The Plant Cell 28:2850−65

    doi: 10.1105/tpc.16.00717

    CrossRef   Google Scholar

    [179]

    Ren Y, Wang Y, Pan T, Wang Y, Wang Y, et al. 2020. GPA5 encodes a Rab5a effector required for post-golgi trafficking of rice storage proteins. The Plant Cell 32:758−77

    doi: 10.1105/tpc.19.00863

    CrossRef   Google Scholar

    [180]

    Liu F, Ren Y, Wang Y, Peng C, Zhou K, et al. 2013. OsVPS9A functions cooperatively with OsRAB5A to regulate post-golgi dense vesicle-mediated storage protein trafficking to the protein storage vacuole in rice endosperm cells. Molecular Plant 6:1918−32

    doi: 10.1093/mp/sst081

    CrossRef   Google Scholar

    [181]

    Fukuda A, Nakamura A, Hara N, Toki S, Tanaka Y. 2011. Molecular and functional analyses of rice NHX-type Na+/H+ antiporter genes. Planta 233:175−88

    doi: 10.1007/s00425-010-1289-4

    CrossRef   Google Scholar

    [182]

    Matsushima R, Maekawa M, Kusano M, Kondo H, Fujita N, et al. 2014. Amyloplast-localized SUBSTANDARD STARCH GRAIN4 protein influences the size of starch grains in rice endosperm. Plant Physiology 164:623−36

    doi: 10.1104/pp.113.229591

    CrossRef   Google Scholar

    [183]

    Gao Y, Xu Z, Zhang L, Li S, Wang S, et al. 2020. MYB61 is regulated by GRF4 and promotes nitrogen utilization and biomass production in rice. Nature Communications 11:5219

    doi: 10.1038/s41467-020-19019-x

    CrossRef   Google Scholar

    [184]

    Zhang Y, Tan L, Zhu Z, Yuan L, Xie D, et al. 2015. TOND1 confers tolerance of nitrogen deficiency in rice. The Plant Journal 81:367−76

    doi: 10.1111/tpj.12736

    CrossRef   Google Scholar

    [185]

    Zhao M, Zhao M, Gu S, Sun J, Ma Z, et al. 2019. DEP1 is involved in regulating the carbon-nitrogen metabolic balance to affect grain yield and quality in rice (Oriza sativa L.). PLoS One 14:e0213504

    doi: 10.1371/journal.pone.0213504

    CrossRef   Google Scholar

    [186]

    Liu Y, Wang H, Jiang Z, Wang W, Xu R, et al. 2021. Genomic basis of geographical adaptation to soil nitrogen in rice. Nature 590:600−5

    doi: 10.1038/s41586-020-03091-w

    CrossRef   Google Scholar

    [187]

    Wu K, Wang S, Song W, Zhang J, Wang Y, et al. 2020. Enhanced sustainable green revolution yield via nitrogen-responsive chromatin modulation in rice. Science 367:eaaz2046

    doi: 10.1126/science.aaz2046

    CrossRef   Google Scholar

    [188]

    Tang W, Ye J, Yao X, Zhao P, Xuan W, et al. 2019. Genome-wide associated study identifies NAC42-activated nitrate transporter conferring high nitrogen use efficiency in rice. Nature Communications 10:5279

    doi: 10.1038/s41467-019-13187-1

    CrossRef   Google Scholar

    [189]

    Gao Z, Wang Y, Chen G, Zhang A, Yang S, et al. 2019. The indica nitrate reductase gene OsNR2 allele enhances rice yield potential and nitrogen use efficiency. Nature Communications 10:5207

    doi: 10.1038/s41467-019-13110-8

    CrossRef   Google Scholar

    [190]

    Hu B, Wang W, Ou S, Tang J, Li H, et al. 2015. Variation in NRT1.1B contributes to nitrate-use divergence between rice subspecies. Nature Genetics 47:834−38

    doi: 10.1038/ng.3337

    CrossRef   Google Scholar

    [191]

    Wang Q, Su Q, Nian J, Zhang J, Guo M, et al. 2021. The Ghd7 transcription factor represses the ARE1 expression to enhance nitrogen utilization and grain yield in rice. Molecular Plant 23:1012−23

    doi: 10.1016/j.molp.2021.04.012

    CrossRef   Google Scholar

    [192]

    Wang Q, Nian J, Xie X, Yu H, Zhang J, et al. 2018. Genetic variations in ARE1 mediate grain yield by modulating nitrogen utilization in rice. Nature Communications 9:735

    doi: 10.1038/s41467-017-02781-w

    CrossRef   Google Scholar

    [193]

    Fang J, Zhang F, Wang H, Wang W, Zhao F, et al. 2019. Ef-cd locus shortens rice maturity duration without yield penalty. Proceedings of the National Academy of Sciences of the United States of America 116:18717−22

    doi: 10.1073/pnas.1815030116

    CrossRef   Google Scholar

    [194]

    Yu J, Zhen X, Li X, Li N, Xu F. 2019. Increased Autophagy of Rice Can Increase Yield and Nitrogen Use Efficiency (NUE). Frontiers in Plant Science 10:584

    doi: 10.3389/fpls.2019.00584

    CrossRef   Google Scholar

    [195]

    Hou M, Luo F, Wu D, Zhang X, Lou M, et al. 2021. OsPIN9, an auxin efflux carrier, is required for the regulation of rice tiller bud outgrowth by ammonium. New Phytologist 229:935−49

    doi: 10.1111/nph.16901

    CrossRef   Google Scholar

    [196]

    Yu J, Xuan W, Tian Y, Fan L, Sun J, et al. 2021. Enhanced OsNLP4-OsNiR cascade confers nitrogen use efficiency by promoting tiller number in rice. Plant Biotechnology Journal 19:167−76

    doi: 10.1111/pbi.13450

    CrossRef   Google Scholar

    [197]

    Wu J, Zhang ZS, Xia JQ, Alfatih A, Song Y, et al. 2021. Rice NIN-LIKE PROTEIN 4 plays a pivotal role in nitrogen use efficiency. Plant Biotechnology Journal 19:448−61

    doi: 10.1111/pbi.13475

    CrossRef   Google Scholar

    [198]

    Hu B, Jiang Z, Wang W, Qiu Y, Zhang Z, et al. 2019. Nitrate–NRT1.1B–SPX4 cascade integrates nitrogen and phosphorus signalling networks in plants. Nature Plants 5:401−13

    doi: 10.1038/s41477-019-0384-1

    CrossRef   Google Scholar

    [199]

    Alfatih A, Wu J, Zhang ZS, Xia JQ, Jan SU, et al. 2020. Rice NIN-LIKE PROTEIN 1 rapidly responds to nitrogen deficiency and improves yield and nitrogen use efficiency. Journal of Experimental Botany 71:6032−42

    doi: 10.1093/jxb/eraa292

    CrossRef   Google Scholar

    [200]

    Wang S, Yang Y, Guo M, Zhong C, Yan C, Sun S. 2020. Targeted mutagenesis of amino acid transporter genes for rice quality improvement using the CRISPR/Cas9 system. The Crop Journal 8:457−64

    doi: 10.1016/j.cj.2020.02.005

    CrossRef   Google Scholar

    [201]

    Wang J, Wu B, Lu K, Wei Q, Qian J, et al. 2019. The Amino Acid Permease 5 (OsAAP5) Regulates Tiller Number and Grain Yield in Rice. Plant Physiology 180:1031−45

    doi: 10.1104/pp.19.00034

    CrossRef   Google Scholar

    [202]

    Lu K, Wu B, Wang J, Zhu W, Nie H, et al. 2018. Blocking amino acid transporter OsAAP3 improves grain yield by promoting outgrowth buds and increasing tiller number in rice. Plant Biotechnology Journal 16:1710−22

    doi: 10.1111/pbi.12907

    CrossRef   Google Scholar

    [203]

    Ji Y, Huang W, Wu B, Fang Z, Wang X. 2020. The amino acid transporter AAP1 mediates growth and grain yield by regulating neutral amino acid uptake and reallocation in Oryza sativa. Journal of Experimental Botany 71:4763−77

    doi: 10.1093/jxb/eraa256

    CrossRef   Google Scholar

    [204]

    Ranathunge K, El-kereamy A, Gidda S, Bi YM, Rothstein SJ. 2014. AMT1;1 transgenic rice plants with enhanced NH4+ permeability show superior growth and higher yield under optimal and suboptimal NH4+ conditions. Journal of Experimental Botany 65:965−79

    doi: 10.1093/jxb/ert458

    CrossRef   Google Scholar

    [205]

    Suenaga A, Moriya K, Sonoda Y, Ikeda A, von Wirén N, et al. 2003. Constitutive expression of a novel-type ammonium transporter OsAMT2 in rice plants. Plant & Cell Physiology 44:206−11

    doi: 10.1093/pcp/pcg017

    CrossRef   Google Scholar

    [206]

    Liu X, Tian Y, Chi W, Zhang H, Yu J, et al. 2022. Alternative splicing of OsGS1;1 affects nitrogen-use efficiency, grain development, and amylose content in rice. The Plant Journal 110:1751−62

    doi: 10.1111/tpj.15768

    CrossRef   Google Scholar

    [207]

    Lal SK, Mehta S, Raju D, Achary VMM, Venkatapuram AK, et al. 2023. Concurrent overexpression of rice GS1;1 and GS2 genes to enhance the nitrogen use efficiency (NUE) in transgenic rice. Journal of Plant Growth Regulation 42:6699−720

    doi: 10.1007/s00344-023-10988-z

    CrossRef   Google Scholar

    [208]

    Lee S, Marmagne A, Park J, Fabien C, Yim Y, et al. 2020. Concurrent activation of OsAMT1;2 and OsGOGAT1 in rice leads to enhanced nitrogen use efficiency under nitrogen limitation. The Plant Journal 103:7−20

    doi: 10.1111/tpj.14794

    CrossRef   Google Scholar

    [209]

    Lee S, Park JH, Lee J, Shin D, Marmagne A, et al. 2020. OsASN1 overexpression in rice increases grain protein content and yield under nitrogen-limiting conditions. Plant & Cell Physiology 61:1309−20

    doi: 10.1093/pcp/pcaa060

    CrossRef   Google Scholar

    [210]

    Wu j, Zhang Z, Zhang Q, Han X, Gu X, Lu T. 2015. The molecular cloning and clarification of a photorespiratory mutant, oscdm1, using enhancer trapping. Frontiers in Genetics 6:226

    doi: 10.3389/fgene.2015.00226

    CrossRef   Google Scholar

    [211]

    Bi Y-M, Kant S, Clark J, Gidda S, Ming F, et al. 2009. Increased nitrogen-use efficiency in transgenic rice plants over-expressing a nitrogen-responsive early nodulin gene identified from rice expression profiling. Plant, Cell & Environment 32:1749−60

    doi: 10.1111/j.1365-3040.2009.02032.x

    CrossRef   Google Scholar

    [212]

    Tang Z, Fan X, Li Q, Feng H, Miller AJ, et al. 2012. Knockdown of a rice stelar nitrate transporter alters long-distance translocation but not root influx. Plant Physiology 160:2052−63

    doi: 10.1104/pp.112.204461

    CrossRef   Google Scholar

    [213]

    Chen J, Fan X, Qian K, Zhang Y, Song M, et al. 2017. pOsNAR2.1: OsNAR2.1 expression enhances nitrogen uptake efficiency and grain yield in transgenic rice plants. Plant Biotechnology Journal 15:1273−83

    doi: 10.1111/pbi.12714

    CrossRef   Google Scholar

    [214]

    Yan M, Fan X, Feng H, Miller AJ, Shen Q, et al. 2011. Rice OsNAR2.1 interacts with OsNRT2.1, OsNRT2.2 and OsNRT2.3a nitrate transporters to provide uptake over high and low concentration ranges. Plant, Cell & Environment 34:1360−72

    doi: 10.1111/j.1365-3040.2011.02335.x

    CrossRef   Google Scholar

    [215]

    Wang W, Hu B, Yuan D, Liu Y, Che R, et al. 2018. Expression of the nitrate transporter gene OsNRT1.1A/OsNPF6.3 confers high yield and early maturation in rice. The Plant Cell 30:638−51

    doi: 10.1105/tpc.17.00809

    CrossRef   Google Scholar

    [216]

    Zhang S, Zhu L, Shen C, Ji Z, Zhang H, et al. 2021. Natural allelic variation in a modulator of auxin homeostasis improves grain yield and nitrogen use efficiency in rice. The Plant Cell 33:566−80

    doi: 10.1093/plcell/koaa037

    CrossRef   Google Scholar

    [217]

    Xu J, Shang L, Wang J, Chen M, Fu X, et al. 2021. The SEEDLING BIOMASS 1 allele from indica rice enhances yield performance under low-nitrogen environments. Plant Biotechnology Journal 19:1681−83

    doi: 10.1111/pbi.13642

    CrossRef   Google Scholar

    [218]

    Yoon DK, Ishiyama K, Suganami M, Tazoe Y, Watanabe M, et al. 2020. Transgenic rice overproducing Rubisco exhibits increased yields with improved nitrogen-use efficiency in an experimental paddy field. Nature Food 1:134−39

    doi: 10.1038/s43016-020-0033-x

    CrossRef   Google Scholar

    [219]

    Zhang M, Wang Y, Chen X, Xu F, Ding M, et al. 2021. Plasma membrane H+-ATPase overexpression increases rice yield via simultaneous enhancement of nutrient uptake and photosynthesis. Nature Communications 12:735

    doi: 10.1038/s41467-021-20964-4

    CrossRef   Google Scholar

    [220]

    Fang Z, Bai G, Huang W, Wang Z, Wang X, et al. 2017. The rice peptide transporter OsNPF7.3 is induced by organic nitrogen, and contributes to nitrogen allocation and grain yield. Frontiers in Plant Science 8:1338

    doi: 10.3389/fpls.2017.01338

    CrossRef   Google Scholar

    [221]

    Liu Q, Han R, Wu K, Zhang J, Ye Y, et al. 2018. G-protein βγ subunits determine grain size through interaction with MADS-domain transcription factors in rice. Nature Communications 9:852

    doi: 10.1038/s41467-018-03047-9

    CrossRef   Google Scholar

    [222]

    Sun H, Qian Q, Wu K, Luo J, Wang S, et al. 2014. Heterotrimeric G proteins regulate nitrogen-use efficiency in rice. Nature Genetics 46:652−56

    doi: 10.1038/ng.2958

    CrossRef   Google Scholar

  • Cite this article

    Lou G, Bhat MA, Tan X, Wang Y, He Y. 2023. Research progress on the relationship between rice protein content and cooking and eating quality and its influencing factors. Seed Biology 2:16 doi: 10.48130/SeedBio-2023-0016
    Lou G, Bhat MA, Tan X, Wang Y, He Y. 2023. Research progress on the relationship between rice protein content and cooking and eating quality and its influencing factors. Seed Biology 2:16 doi: 10.48130/SeedBio-2023-0016

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Research progress on the relationship between rice protein content and cooking and eating quality and its influencing factors

Seed Biology  2 Article number: 16  (2023)  |  Cite this article

Abstract: Proteins, the second-largest storage substance in rice endosperm, play an important role in determining the cooking and eating qualities of rice. Its contents are influenced by both genetic and environmental factors. This article provides a review of the evaluation methods for cooking and eating qualities of rice and starch physicochemical properties, the factors that affect the protein content of rice, the genetic basis of rice protein content, the research progress made in the genetic improvement of rice protein content, and the prospects for the future, aiming to provide a reference for the genetic improvement of rice protein content and the breeding of rice varieties with excellent taste.

    • Rice yield and quality have always been of concern as it is one of the main food crops worldwide. The rice yield greatly improved after the two green revolutions. However, research and breeding practices related to rice quality lag far behind those focused on rice yield. This may reflect the neglect of rice quality in the past, complexity of rice quality research, and lack of a consensus definition and evaluation criteria for rice quality. Rice quality is a complex character based on several evaluation indices that reflect both internal and external attributes, such as appearance, taste, and flavor. Rice quality encompasses various qualities, such as appearance, milling, nutritional value, cooking and eating, and sanitary qualities[1]. Rice quality, especially appearance, cooking, and eating quality, plays a crucial role in determining consumer preference and commercial value. Undoubtedly, rice with excellent appearance and taste is more likely to be favored by consumers.

      Rice quality is mainly determined by the synthesis, composition, distribution, and accumulation of nutrients and storage products. Cooking and eating quality are important indicators of many quality traits. Currently, in breeding practice, improving the taste quality of rice relies primarily on allelic variations in the waxy gene Wx, encoding granule-bound starch synthase I (GBSSⅠ). This allows the cultivation of rice varieties with varying amylose contents to meet the needs of different consumer groups[29].

      Wx is known to control amylose synthesis in rice endosperm. In addition to its direct function on amylose synthesis, the Wx gene interacts with many other genes, both directly and indirectly. These interactions regulate the expression level of Wx and ultimately impact the amylose content and quality of rice. The regulation occurs at the transcriptional and post-transcriptional levels, and also involves interactions with GBSSI proteins, as well as some unknown forms of interaction. Certain genes or QTL (Quantitative trait loci), such as Du1[10], Du3[11], Du13[12], FLO2[13], qAC2[14], qSAC3[15], and LowAC1[16], have been reported to manipulate Wx mRNA splicing efficiency, directly controlling the amylose content in rice grains. Additionally, certain transcription factors like OsNAC24[17], OsNAC20[18], OsNAC26[18], OsNF-YB1[19], OsNF-YC12[9], bHLH144[15], OsMADS7[20], OsMADS14[21], OsBP-5[22], OsEBP-89[22], REB[23], and OsbZIP60[24] have been found to regulate the expression of Wx gene in rice endosperm, either directly or indirectly. There are also some quality genes, such as OsAAP6[25], Chalk5[26], WCR1[27], FLO19[28], that affect the expression level of Wx genes in unknown ways. Furthermore, OsGBP[29] and FLO6[30] have been discovered to be involved in starch synthesis through direct interaction with GBSSI. Exploring natural variations of these genes that interact with Wx, or modifying these genes themselves through genetic engineering, are potential strategies for enhancing the quality of cooked rice.

      The Wx gene not only affects the synthesis of endosperm starch and the physicochemical properties of starch[31], but also has a powerful pleiotropic function that impacts the quality of rice from multiple aspects. Tan et al. identified a major protein content QTL in the Wx gene region, which is also responsible for flour color[32]. Chen et al. investigated the total protein content and four storage protein contents of 527 rice germplasms using a genome-wide association study, and discovered that the distance between an association site with a phenotypic variation rate greater than 10% and the quality gene Wx was less than 20 Kb[33]. By conducting haplotype analysis and endosperm expression analysis of the Wx gene, they observed that the 2.3 kb mRNA level of Wx was inversely proportional to the albumin content[33]. This finding further supports the conclusion that Wx is a gene responsible for endosperm protein content. In 2020, two different research groups almost simultaneously reported that Wx also regulates grain transparency and eating quality[8,9]. According to Xia et al.'s genome-wide association studies, it was discovered that the Wx gene acts as a negative regulator for both crude fatty acid content and rice quality[34,35]. Qiu et al. showed that Wx gene is highly correlated with cooked rice elongation[36]. Deng et al.'s research highlighted the significance of the Wx gene in regulating grain fissure resistance, and its genetic variation conferred different levels of tolerance to fissuring in grains as well as head rice yield[37]. Thus, Wx does not affect rice quality solely by controlling amylose synthesis, but rather depends on its pleiotropic effects, which determine the overall quality of rice from various perspectives (Fig. 1).

      Figure 1. 

      Pleiotropy of Wx gene in rice quality regulation. This pattern diagram presents the regulatory factors of the Wx gene at both the transcriptional and post-transcriptional levels that have been reported thus far. It also highlights the encoding product GBSSI of the Wx gene, which plays a role in regulating the three major components of rice endosperm (starch, protein, and lipids) and subsequently affects various physicochemical properties of rice grains. The pleiotropic effect of the Wx gene ultimately determines the overall quality of rice from multiple perspectives. GC, gel consistency; GT, gelatinization temperature. Yellow spheres with the letter P indicate phosphorylation.

      Although significant progress has been made in improving the quality of rice with regard to starch, the quality of the existing rice still fails to meet the diverse needs of consumers. Proteins have attracted the attention of rice quality researchers because they are the second-largest storage substances in rice, after starch. Proteins in rice can be divided into two categories according to their functions: storage and structural proteins. Most of the proteins in rice seeds are storage proteins, whereas structural proteins are responsible for maintaining normal cell metabolism, mainly hormones, enzymes, and enzyme inhibitors, and their total content is relatively small[38]. Therefore, rice proteins are generally referred to as storage proteins. Studies have shown that rice seed storage proteins are mainly distributed in the aleurone layer and embryo[39]. Albumin and globulin are more abundant in the aleurone and glume layers. Glutelin is the most abundant protein in the endosperm, and albumin is evenly distributed in rice bran, fine bran, and milled rice[40]. The storage proteins in the endosperm are mainly filled between starch granules in the form of independent proteomes (PBs), which can be divided into two types: spherical type I proteomes (PB-I) with concentric lamellar structures and elliptical type II proteomes (PB-II) without lamellar structures. PB-I mainly contains prolamin, accounting for approximately 20%–30% of the total endosperm storage protein[41]. PB-II is mainly composed of glutelin with a small amount of globulin, accounting for approximately 65% of the total stored protein in endosperm[42]. Glutelin is the first major component of rice grain storage protein[43]. To date, research on the biosynthesis and genetics on glutelin has been the most common. In this regard, there have been two excellent reviews[40,44] on the progress in rice glutelin biosynthesis and genetics, which will not be repeated here.

      The protein content and composition of rice also seriously affect various quality traits, particularly the cooking and eating quality.

      Singh et al. found that the gelatinization characteristics of rice flour and starch from the same variety were different, suggesting that factors other than starch affect the gelatinization process of rice[45]. Martin & Fitzgerald found that during the early stage of cooking, protein reduced the water absorption of rice by binding water and increased the concentration of starch gel in both dispersed and viscous phases through a disulfide-linked protein network, resulting in an increase in the peak viscosity of RVA spectra[46]. Hamaker & Griffin used the reducing agent dithiothreitol (DTT) to break the protein disulfide bond and observed significant swelling of the starch granules and an increase in peak viscosity[47,48]. After adding protease or DTT to the rice flour and non-glutinous rice flour, Xie et al. found that the peak viscosity, disintegration value, and recovery value of glutinous rice decreased significantly, indicating that the protein network formed by disulfide bonds enhances the gelatinization rigidity of glutinous rice flour. In contrast, the disintegration value of non-glutinous rice increases without disulfide bonds, and the expansion process of starch particles became more gelatinized[49]. Chavez-murillo et al. reported a significant negative correlation between rice protein, peak viscosity, and disintegration value in RVA, suggesting that proteins affect these indices by binding to water[50]. Baxter et al. added four protein components to pure starch and found that the addition of glutenin and albumin increased the starch gelatinization temperature, whereas the addition of globulin decreased it[51]. The albumin content showed a linear and positive correlation with the hardness of the starch gel and a negative correlation with adhesion. The addition of prolamin to the starch gel results in decreased hardness, adhesion, and adhesive properties. Furthermore, an increase in the prolamin content led to a decrease in both hardness and adhesion[52]. Zhou et al. hydrolyzed the protein in rice with protease and observed that during gelatinization, the number of starch molecules leached and water permeability increased, and the heat absorption temperature of gelatinization decreased, suggesting that protein is an important factor that affects the thermodynamic properties of stored rice[53]. Moreover, many studies have demonstrated that a higher endosperm protein content increases the hardness and roughness of rice and reduces its adhesion and smoothness[54,55]. Existing studies have generally found that the higher the protein content, the worse the cooking and eating quality of rice[56,57]. In summary, the protein content and composition of rice are closely related to its cooking and eating quality.

      This review mainly focuses on the evaluation methods of rice cooking and eating quality and starch physicochemical properties, factors affecting rice protein content, the genetic basis of rice protein content, progress made in the genetic improvement of rice protein content, and future prospects in this field.

    • The evaluation methods for rice taste include instrumental, artificial sensory, physical, and chemical index evaluation methods. At present, the most widely used instrument in rice taste evaluation is the rice taste value analyzer produced by the SATAKE Company in Japan[58]. The instrument can calculate physical parameters, such as viscosity, elasticity, hardness, and balance, by measuring the light characteristics of rice. Based on these measurements, the instrument calculates the taste value of rice using a formula[59]. Sensory evaluation is the most accurate and direct manifestation of the taste quality of rice. After the rice is steamed and cooked under standardized and unified conditions, the evaluators comprehensively evaluate the color, odor, taste, viscosity, softness, hardness, and overall palatability of the tested rice using visual, nasal, and oral methods.

      In addition to these two methods, physical and chemical index evaluation methods are widely used in the evaluation of rice quality and breeding of high-quality rice. The main physical and chemical indices involved include the amylose content, fine structure of amylopectin, gelatinization properties, texture characteristics, and thermodynamic properties (Fig. 2). Amylose content is considered the most important factor in determining rice quality[31,6062]. Therefore, the effects of amylose on rice quality have been extensively and comprehensively studied, which has been summarized in detail in some excellent reviews[1,6264] and will not be repeated here.

      Figure 2. 

      Determinants of cooking and eating quality of rice and external factors affecting protein content of rice grains. The six parts in the inner circle represent the physical and chemical characteristics or indicators that determine the cooking and eating quality of rice; the three parts in the outer circle represent the material composition that affects the physical and chemical characteristics of rice; the cartoon diagram in the outermost circle represents the ecological factors and environmental factors that affect the grain protein content, from clockwise from 1 o'clock to indicate light, moisture, carbon dioxide, salinity, cultivation, fertilizer and temperature.

      Amylose is a very small, linear, or slightly branched structure, whereas amylopectin is a highly branched component of starch. The difference in the eating quality of rice with the same amylose content is generally considered to be closely related to the fine structure of amylopectin. Amylopectin accounts for a large proportion of the starch in the rice endosperm, approximately 70%–90%, and its molecular weight is relatively large. It is generally composed of thousands of glucose residues. There are many non-reducing ends in the molecule, but only one reducing end. The fine complex structure of amylopectin is initially evident over a wide range of chain lengths. The amylopectin chain is divided into A, B, and C chains based on the branch point and degree of polymerization. The reducing end of the A chain is involved in the formation of α-1,6 glycosidic bonds. The reducing end of the B chain is connected to the C chain or the other B chains, and the C chain is the only macromolecule with a reducing end. Depending on the length of the chain, it can be divided into main short chain (generally 0–35 DP) and secondary long chain (generally greater than 35 DP), A chain (6 ≤ DP ≤ 12), B1 chain (13 ≤ DP ≤ 24), B2 chain (25 ≤ DP ≤ 36), B3 chain (DP ≥ 37), and some amylopectin molecules have extra-long chains (EL chains). Second, the fine and complex structure of amylopectin is also evident in the multilevel structure of the starch granules. Amylose and amylopectin aggregate and twist to form a double helix and then aggregate to form different types of crystals. The crystals form amorphous sheets alternately. In addition, crystalline sheets form periodic shell-shaped or ring-shaped growth rings, small starch granules have raised elastic bodies on the surface, and these small starch granules further fused to form composite starch granules.

      The gelatinization properties of rice flour can be characterized by measuring the change in the viscosity of the starch suspension during heating and cooling. During heating, the viscosity gradually reaches a maximum value with increasing temperature and then gradually decreases. which is a function of the change in starch granules[65]. During the cooling process, the viscosity of the starch paste increases over time, which indicates that the gelatinized starch was recycled[66]. Currently, rapid viscosity analyzer (RVA) is mainly used to investigate the gelatinization properties of starch. The RVA gelatinization curve provides several important parameters: the gelatinization temperature (PM), which is the temperature at which starch begins to gelatinize; peak viscosity (PV), which represents the maximum viscosity of starch particles before breaking; peak time (PT), which indicates the time when starch reaches peak viscosity; decay value (BD), which indicates the stability of starch hot paste under shear stress; retrogradation value (SB), indicating that the gelatinized starch paste begins to retrograde when cooled; and final viscosity (FV), which represents the final viscosity of the RVA curve[67].

      Texture properties, such as hardness, brittleness, stickiness, resilience, elasticity, and gel strength, are important food quality factors. Sensory evaluation is a highly recognized evaluation method; however, it has some limitations, such as strong subjectivity and being greatly influenced by the evaluator's own preferences. In this context, a texture instrument has been developed to replace human sensory evaluation and provide specific index parameters. A texture tester, also known as a physical property tester, is mainly used to simulate the mechanical movement of oral chewing. The most commonly used test is the texture profile analysis (TPA) program, which is also known as the secondary extrusion cycle or twice mastication test (two-bite test, TBT). By simulating the chewing movement of the human cavity, a solid or semi-solid sample is extruded twice to obtain texture parameters.

      Starch gelatinization is an irreversible process that includes granule swelling, crystal dissolution, loss of birefringence, and starch dissolution, accompanied by changes in viscosity. The phase transition of starch granules involves the expansion and rupture of starch granules. The gel temperature is the key point of these two stages because it is at this point that the impact on the rupture of starch granules is the greatest. The temperature parameters of the starch gelatinization process can be determined by differential scanning calorimetry, including the degree of crystallization, transition effect, and melting point of starch during the gelatinization reaction, as well as the degree of gelatinization and recovery characteristics of starch.

    • As a typical quantitative trait, phenotypic differences in rice protein content among different genotypes are greatly affected by the environment. Ecological factors, such as temperature, light, and carbon dioxide concentration, and environmental factors, such as cultivation, affect the protein content of rice (Fig. 2).

      Rice is a typical temperature-loving crop, and the protein content of the grain is very sensitive to temperature changes during the grain-filling stage. High temperatures during the filling stage usually lead to an increase in grain protein content, decrease in amylose content and taste value, and a decrease in grain quality[68]. The high temperature during the mature stage leads to abnormal rice quality, shape, and color, which may be attributed to a decrease in enzyme activity, respiratory consumption of assimilation products, and reduced sink activity related to grain filling[69,70].

      Light, in addition to temperature, is another key factor that affects protein synthesis. It has been found that the main protein components, such as glutelin, and the most important essential amino acids, including lysine and threonine, increased significantly in rice harvested after low-light treatment at the filling stage; however, cooking quality decreased[71].

      Some studies have shown that the atmospheric concentration of CO2 has an important effect on rice quality. Goufo et al. demonstrated that elevated carbon dioxide levels result in reduced protein content in plants, which is attributed to the inhibition of nitrate assimilation[72,73]. Furthermore, the researchers observed an increase in peak viscosity, minimum viscosity, breakdown value, final viscosity, and hardness of rice, while noting a decrease in setback value. All these alterations in physical and chemical indicators collectively indicate an enhancement in the cooking and eating quality of rice[72].

      Moisture and fertilizer are the two most important factors in cultivation management. In many systems, 5,000 liters of water is required to produce 1 kg of rice, although this can be reduced to approximately 2,000 liters[74]. Soil moisture status has a significant impact on yield and grain quality[75]. Rice is generally grown under submerged conditions. Submerged plastic film mulching (PM) and submerged wheat straw mulching (SM) are emerging water-saving technologies for rice production. Different water management treatments, namely PM, water-saving grouting, and conventional irrigation, significantly affected the percentage of brown rice, milled rice, chalky grain, amylose content, and protein content in a variety- and grain-position-dependent manner. The protein content is the most affected by water management[76]. Nitrogen is crucial for plant growth and development. As nitrogen is still the main component of proteins, applying nitrogen fertilizer can also significantly affect the quality of grains[35,77]. The application of nitrogen fertilizer at different stages of panicle differentiation, heading, flowering, and grain filling could significantly increase the content of grain storage protein[78]. In addition to nitrogen, potassium is another fertilizer necessary for rice production. Some studies have shown that the application of potassium fertilizer increased gel consistency and grain protein content but had no significant effect on gelatinization temperature and amylose content[79].

      Salinity is another important factor that significantly influences crop quality. By comparing rice varieties grown in low-and high-salinity areas, Siscar-Lee et al.[80] found that salt-tolerant and salt-sensitive varieties grown in saline-alkali soil had higher storage protein content than those grown in normal soil; however, these varieties also had less translucent grains and lower starch and amylose contents[80]. Owing to the significant influence of the environment, the interaction between the protein content genotype and the environment is large, and the heritability is relatively small. Some studies have shown that the heritability of the phenotype of protein content in rice is only 13.0% and 37.2%[81]; therefore, the phenotype with high protein content has little effect in the early generation. However, it is also reported that its heritability can reach 58.8%[82]. Therefore, it is feasible to screen materials with high protein content in the lower generation. Several external factors aggravate the complexity and challenge of rice protein research.

    • Rice grain protein content is a quality trait controlled by multiple genetic factors with a complex genetic basis. There are large differences in the protein content among the different varieties[83]. Chen et al. determined the grain protein content of 527 cultivated rice core germplasm and showed that the protein content ranged from 44.06 to 106.71 mg/g in 2014 and 32.64 to 80.08 mg/g in 2015[33]. Similarly, Yang et al. used near-infrared spectroscopy to measure the protein content of 402 core germplasms. The two-year phenotypic data showed that the protein content of rice varied from 5.33% to 14.83%, and the protein content of most varieties was distributed between 7.5% and 11.5%[83]. Liu et al. measured the protein content of 24 japonica rice varieties collected from different regions in China and found that the protein content ranged from 6.45% to 11.1%, with an average of 8.26%[84]. Webb et al. analyzed the protein content of approximately 4,000 rice varieties from 57 countries and found that the protein content ranged from 5.3% to 13.6%[85].

    • To date, numerous studies have mapped quantitative trait loci (QTL) that control the protein content of rice. Tan et al. used a set of recombinant inbred line populations to detect a QTL related to protein content on chromosomes 6 and 7 respectively, one of these QTLs was located near Wx on chromosome 6 and had a large effect, explaining 13.0% of the phenotypic variation[32]. Aluko et al. used DH populations derived from BC3F1 (O. sativa × O. glaberrima) to detect QTL controlling protein content on chromosomes 1, 2, 6, and 11, respectively[86]. Similar to the results obtained by Tan et al., the QTL on chromosome 6 had the largest effect and was located near the Wx gene[86]. Hu et al. also used a DH population (Gui630×02428) and identified five QTLs for rice protein content, among which the QTL effect on chromosome 5 in RG435-RG172a was found to be the largest[87]. Kepiro et al. used an RIL population to map QTLs related to protein content in both brown rice and milled rice respectively[88]. They observed that the two loci were located in brown rice and three loci were located in milled rice. The loci on chromosomes 1 and 4 simultaneously control the protein content of brown rice and milled rice[88]. Wang et al. used the RIL population (Zhenshan97/Nanyangzhan) to map QTLs for different amino acid contents and found that there was a QTL with a large effect at the end of the long arm of rice chromosome 1 that simultaneously controlled the contents of multiple amino acids[89]. Using the RIL population constructed by Chuan 7 and Nanyangzhan, Luo et al. detected two QTLs affecting protein content; however, the effects of these QTLs were small, and phenotypic variation explained only 7.2%[90]. Ye et al. detected at least 15 fragments related to protein content using two-year data of chromosome segment substitution line (CSSL) populations at four sites, among which CSSL-48 on chromosome 8 was detected in all eight environments[91]. Liu et al. mapped nine protein content-related QTL on chromosomes 1, 2, 3, 6, 8, and 11 using a CSSL (Asominori × IR24) population[92]. Bruno et al. identified a minor QTL for brown rice protein content on chromosome 7, using a set of DH populations[93]. Kashiwagi & Munakata used a set of single-segment substitution line populations obtained from crosses between Koshihikari and NonaBokra to identify a stably inherited QTL, TGP12, which controls the protein content of rice across three years of different environments[94]. This QTL can specifically reduce protein content of rice without affecting its cooking and eating quality[94]. Park et al. used a set of RIL populations obtained from the crossing parents with large differences in rice quality, and identified a stable genetic QTL qPro9 on chromosome 9 through 2 years of repeated identification, and fine-mapped it to a specific region of 34 Kb[95]. Zhang et al. studied the inheritance of crude protein and its components in rice using 71 recombinant inbred lines (RIL) obtained from crossing the japonica rice variety Asominori with indica rice variety IR24[96]. They identified a total of 16 QTLs located on eight chromosomes[96]. To investigate the genetic relationship between rice yield and rice nutrient content, Yu et al. used 209 recombinant inbred lines obtained from crossing XieqingzaoB with Milyang46 to map the QTL that affects brown rice yield and two main nutrient contents. Five QTLs related to protein content were detected on chromosomes 3, 4, 5, 6, and 10. Among them, a major QTL qPC-6 was located near the Wx marker RM190 on the short arm of rice chromosome 6, which explains 19.3% of the phenotypic variation with an additive effect of 0.471%[97]. Zheng et al. used 71 lines derived from 'Asominori/IR24' to analyze the developmental behavior of protein content and protein index (PI) through unconditional and conditional QTL mapping. Ten unconditional QTLs, six conditional QTLs of proteins, 11 unconditional QTLs, and nine conditional QTLs of PI have been identified at four stages of grain filling[98].

      Advanced molecular breeding methods, such as genome-wide association analysis (GWAS), supported by next-generation sequencing and omics technology, can effectively identify genomic regions related to rice quality traits[99102]. Thus, in addition to using parental-derived genetic populations to identify QTLs related to rice protein content, researchers have also attempted to use natural populations of rice to conduct GWAS to find genes/QTLs related to protein content of rice. Chen et al. conducted GWAS of total protein content and four stored protein contents of 527 rice varieties in the overall population, as well as in the indica rice subpopulation and japonica rice subpopulation. They detected a total of 107 significant association loci, of which 28 loci overlapped with reported QTLs or intervals known to control rice protein content. Sixteen loci were detected in different populations and nine of them were simultaneously detected in different phenotypes. Based on the analysis of the associated loci that explained a phenotypic variation rate of more than 10%, 13 loci were found to be co-located with genes related to quality, and the distances between 5 loci and quality-related genes (PG5a, Wx, AGPS2a, RP6, and RM1) were less than 20Kb[33]. Similarly, 135 significant loci related to grain protein content have been identified through genome-wide association studies[103], among these loci, six leading SNPs are located near the known genes involved in the biosynthesis and accumulation of storage proteins (less than 150 Kb), including Sar1a, GluB6, OsTudor-SN, and Glb1. In addition, two genes (Susy2 and Flo5), which have been shown to play a key role in rice starch synthesis, are less than 50 Kb from the leading SNPs, and the chalkiness rate and protein content of mutants obtained by editing Flo5 are significantly higher than those of the wild type[103]. Yang et al. used a population of CSSLs obtained by crossing the indica rice variety Habataki with japonica rice variety Sasanishiki for QTL mapping and identified 18 QTLs related to grain protein content across three environmental conditions. Among these, qGPC-1 and qGPC-10 were repeatedly identified in all three environmental conditions, whereas qGPC-3, qGPC-8, and qGPC-12 were detected under both environmental conditions, and the others could only be detected under one environmental condition[83]. Huang et al. conducted a genome-wide association study on heading date and ten grain-related traits, of 950 rice varieties worldwide using a high-density haplotype map to identify five candidate genes for grain protein content on chromosomes 6, 7, and 11, in combination with expression profile data and gene annotation information[104]. Verma et al. used 42,446 SNP markers to perform a genome-wide association study on five grain quality traits of 103 rice varieties and identified multiple grain protein QTLs on chromosomes 1, 2, 6, 7, 10, and 11[105]. Moreover, a novel grain protein QTL, qPRO_1.12 was identified on chromosome 12[105]. Using different sets of 258 germplasm from the 3 K Rice Genome Project, Wang et al. conducted an association study on apparent amylopectin content (AAC), gel consistency (GC), gelatinization temperature (GT), and PC in two environments, and detected three QTLs affecting protein content[106].

    • Although many QTLs have been identified and reported, cloning QTLs related to protein content has become extremely difficult owing to various influencing factors. To date, only a limited number of genes have been cloned from natural populations, which can be used for quality improvement. Peng et al.[25] cloned the first protein content gene, OsAAP6, in rice, which encodes an amino acid transporter and functions as a positive regulator of the storage protein content. Upregulation of its expression can increase the contents of the four storage proteins. Notably, the OsAAP6 allele from Nanyangzhan reduced the content of the four storage proteins while improving the cooking quality of rice. In 2019, Yang et al.[83] cloned a major glutelin gene, OsGluA2, which acts as a positive regulator of rice protein content. The higher the expression level, the higher the glutelin content and the larger the volume of protein body II. In addition, a large number of floury endosperm genes may also affect grain protein content and (Table 1), but previous researchers did not pay enough attention.

      Table 1.  Reported floury endosperm genes that may affect grain protein content.

      ClassificationNameGene IDEffect of gene knockout
      or knockdown on grain
      protein content
      Annotation
      Biochemical metabolismflo4/OsPPDKB/OsC4PPDKLOC_Os05g33570Increased[130]Pyruvate, phosphate dikinase
      OsSSIIIa/Flo5/SS3aLOC_Os08g09230Increased[103]Starch synthase III
      FLO8/OsUgp1LOC_Os09g38030Increased[131]UTP--glucose-1-phosphate uridylyltransferase
      FLO12/OsAlaAT1LOC_Os10g25130Increased[132,133]Aminotransferase
      FLO15/OsGLYI7LOC_Os05g14194Increased[134]Glyoxalase family protein
      FLO16LOC_Os10g33800Increased[135]lactate/malate dehydrogenase
      FSE1LOC_Os08g01920Increased[136]Phospholipase-like protein
      OsAGPL2/OsAPL2/shr1/GIF2/osagpl2-3LOC_Os01g44220Decreased[137]ADP-glucose pyrophosphorylase large subunit 2
      OsBEIIb/be2bLOC_Os02g32660Unknown[138]Starch branching enzyme IIb
      Pho1LOC_Os03g55090Unknown[139]Plastidial phosphorylase
      OsGINT1/FSE6LOC_Os05g46260Increased[140]Glycosyltransferase
      OsPK2/OsPKpα1LOC_Os07g08340Increased[141]Plastidic pyruvate kinase
      GIF1/OsCIN2LOC_Os04g33740Unknown[142]Glycosyl hydrolases
      PDIL1-1LOC_Os11g09280Increased[143]Protein disulphide isomerase-like enzyme
      OsACS6/SSG6LOC_Os06g03990Unknown[144]Aminotransferase
      PFPβ/PFP1LOC_Os06g13810Unknown[145]Pyrophosphate-fructose 6-phosphate
      1-phosphotransferase subunit beta
      FLO19LOC_Os03g48060Increased[28]Class I glutamine amidotransferase
      FLO19LOC_Os04g02900Decreased[146]Plastid-localized pyruvate dehydrogenase complex E1 component subunit α1
      FLO23/OsF2KP2LOC_Os03g18310Decreased[147]Fructose-6-phosphate-2-kinase/fructose-2, 6-bisphosphatase
      OsDPE1LOC_Os07g43390Unknown[148]Disproportionating enzyme
      Transcriptional regulation and protein interactionOsNF-YC12LOC_Os10g11580Increased[19,149]CCAAT-box-binding transcription factor
      OsNF-YB1/OsHAP3K/OsEnS-41LOC_Os02g49410Increased[19]Nuclear transcription factor Y subunit B
      bHLH144LOC_Os04g35010Increased[19]Helix-loop-helix DNA-binding domain containing protein
      RISBZ1/OsbZIP58LOC_Os07g08420Decreased[150]bZIP transcription factor
      REB/OsbZIP33/RISBZ2LOC_Os03g58250Unknown[151]bZIP transcription factor
      RPBF/OsDof3/OsDof-10/OsDof7LOC_Os02g15350Decreased[150,152]Dof transcription factor
      FLO2LOC_Os04g55230Unknown[153]Tetratricopeptide repeat domain containing protein
      FLO6LOC_Os03g48170Increased[154]CBM48 domain-containing protein
      OsGBPLOC_Os02g04330No change[29]GBSS-binding protein
      FLO7LOC_Os10g32680Unknown[155]DUF1388 domain protein
      OsHsp70cp-2/cpHSP70-2/ flo11-2/ FLO11LOC_Os12g14070Unknown[156]Plastid heat shock protein 70
      RSR1LOC_Os05g03040Unknown[157]Transcription factor of the AP2/EREBP family
      OsNAC20; OsNAC26LOC_Os01g01470; LOC_Os01g29840Decreased when knock out together[18]NAC transcription factor
      OsNAC23/ONAC023LOC_Os02g12310Decreased when gene knock out and increased when gene overexpression[158]NAC transcription factor
      OsNAC24/OsNAC024LOC_Os05g34310Unknown[17]NAC transcription factor
      OsNAC127LOC_Os11g31340Unknown[159]NAC transcription factor
      OsNAC129LOC_Os11g31380Unknown[159,160]NAC transcription factor
      Du13/TL1LOC_Os06g48530No change[12]C2H2 zinc finger protein
      OsbZIP60/O3/OPAQUE3LOC_Os07g44950Decreased[24]Basic leucine zipper transcription factor
      OsMADS6/MFO1LOC_Os02g45770Increased[161]MADS-box transcription factor
      OsMADS29LOC_Os02g07430Unknown[162]MADS-box transcription factor
      OsMADS14LOC_Os03g54160Unknown[21]MADS-box transcription factor
      EpigeneticsOsROS1/ROS1a/DNG702LOC_Os01g11900Increased[163]DNA demethylase
      OsCADT1/FLO20/SHMT4LOC_Os01g65410Decreased[164]Serine hydroxymethyltransferase
      Energy supplyFLO10LOC_Os03g07220Increased[165]Pentatricopeptide repeat protein
      FLO14/OsNPPR3LOC_Os03g51840Unknown[166]Pentatricopeptide repeat protein
      FLO18LOC_Os07g48850Decreased[167]Pentatricopeptide repeat protein
      OGR1LOC_Os12g17080Unknown[168]Pentatricopeptide repeat–DYW protein
      FGR1/OsNPPR1LOC_Os08g19310Unknown[169]Pentatricopeptide repeat protein
      FLO13/OsNDUFA9LOC_Os02g57180Unknown[169]Mitochondrial complex I subunit
      FLO22LOC_Os07g08180Unknown[170]P-type pentatricopeptide repeat (PPR) protein
      Material transportESG1LOC_Os04g46700Decreased[171]Bcterial-type ABC (ATP-binding cassette) lipid transporter
      OsBT1LOC_Os02g10800Unknown[172]ADP-Glucose Transporter
      OsBip1/BiP3LOC_Os02g02410Decreased[173]Endoplasmic riculum caperone
      OsLTPL36LOC_Os03g25350Decreased[174]Lipid transfer protein
      OsRab5a/gpa1/glup4LOC_Os12g43550No change, but pro-glutelin accumulation[175]Small GTPase
      Sar1a; Sar1b; Sar1cLOC_Os01g23620; LOC_Os12g37360; LOC_Os01g15010Unknown but pro-glutelin accumulation when three genes knockdown together[176]Small GTPase
      GPA3LOC_Os03g61950Increased and pro-glutelin accumulation[177]Regulator of post-Golgi vesicular Traffic
      GPA4/GLUP2/GOT1BLOC_Os03g11100Decreased but pro-glutelin accumulation[178]Golgi Transport 1
      GPA5LOC_Os06g43560Unknown but pro-glutelin accumulation[179]Rab5a Effector
      OsVPS9A/GPA2/GLUP6/GEFLOC_Os03g15650Decreased but pro-glutelin accumulation[180]Guanine nucleotide exchange factor
      GPA6/OsNHX5LOC_Os09g11450No change, but pro-glutelin accumulation[181]Vacuolar Na+/H+ antiporter
      Function unknownSSG4LOC_Os01g08420Unknown[182]Unknown function protein
    • Rice grain nitrogen is primarily derived from the nitrogen absorbed from the soil. Therefore, in addition to the external factors, the ability of rice to absorb, transport, assimilate, distribute, and even reuse nitrogen may cause changes in the nitrogen (protein) content of the final grain (Fig. 3). In other words, the nitrogen utilization capacity of rice may also be an internal cause of the difference in grain protein content. Therefore, attention should be paid to genes related to nitrogen use efficiency in rice, as they may also be potential targets for the genetic improvement of rice proteins. In a recent study, Zhang et al. utilized the promoter of the Nhd1 gene to develop rice genetic materials with significantly increased endogenous expression levels[107]. There were no significant changes observed in the entire length of growth duration, nitrogen use efficiency and rice yield of the Nhd1 enhanced line. However, the starch granules in the rice showed a more relaxed arrangement, with noticeable reductions in amylose and protein content. This resulted in a lower gelatinization temperature and increased gel consistency, suggesting that the rice is easier to cook, digest, and has an improved taste. The GRF4 gene is a positive regulator of plant carbon and nitrogen metabolism that can simultaneously promote nitrogen absorption, assimilation, and transport, thereby increasing the total nitrogen level in the grain[108]. LNUE1 gene encodes OsAlaAT1, an alanine aminotransferase that regulates nitrogen use efficiency of rice. lune1 mutant has low nitrogen use efficiency, decreased total protein levels in seeds, and severe chalkiness in the endosperm[109]. THP9[110], the first major gene cloned from wild maize to control the high protein content and NUE of maize, encodes asparagine synthetase 4 (ASN4), which is a key component of nitrogen metabolism and is responsible for asparagine synthesis. Transgenic expression of THP9-teosinte in B73 inbred lines significantly increases seed protein content. The OsDREB1C[111] gene drives a wide range of transcriptional activities that regulate the photosynthetic capacity, nitrogen use efficiency, and heading date of rice. Overexpression of the gene enhanced the ability of rice to absorb and transport nitrogen, allocate more nitrogen to the grain, and increase nitrogen use efficiency by 25.8%–56.6% compared with the control group. In view of the fact that the NUE genes cloned and discovered in many studies currently only have yield data, and relevant researchers have not yet investigated whether these genes also affect grain protein content and quality traits, we collected and summarized the relevant information on the currently known NUE genes (Table 2). This compilation will facilitate further exploration of the effects of these genes on rice grain protein content and quality.

      Figure 3. 

      The nitrogen utilization ability of rice may determine the protein content of grains. Each step of nitrogen utilization in rice, which includes absorption, transportation, assimilation, distribution, and reuse, can potentially impact the final grain protein content.

      Table 2.  Reported nitrogen use efficiency genes that may also affect grain protein content.

      NameGene IDEffect of altered gene function on grain protein contentAnnotation
      MYB61/qNLA1/qCel1LOC_Os01g18240Unknown[183]MYB family transcription factor
      OsGRF4/GS2/GL2/PT2/LGS1/GLW2LOC_Os02g47280Increased when gene overexpression[108]Growth-regulating factor
      TOND1LOC_Os12g43440Unknown[184]Unkonwn function protein
      OsDEP1/DN1/qPE9-1/qNGR9LOC_Os09g26999No change when gene overexpression[185]Gγ subunit
      OsTCP19LOC_Os06g12230Unknown[186]Class-I TCP transcription factor
      SMOS1/shb/RLA1/NGR5LOC_Os05g32270Unknown[187]GRAS protein
      OsNPF6.1LOC_Os01g01360Unknown[188]Nitrate transporter
      OsNAC42LOC_Os09g32040Unknown[188]No apical meristem protein
      OsNR2/qCR2LOC_Os02g53130Unknown[189]Nitrate reductase
      OsNRT1.1B/OsNPF6.5/qCHR-10LOC_Os10g40600Unknown[190]Peptide transporter PTR2
      Ghd7/E1/Hd4LOC_Os07g15770Unknown[191]CCT motif family protein
      ARE1LOC_Os08g12780Unknown[192]Chloroplast envelope membrane protein
      OsCCA1/OsLHY/Nhd1LOC_Os08g06110Decreased when gene expression enhanced[107]MYB transcription factor
      Ef-cdUnknown[193]Long noncoding RNA
      OsAtg8/OsATG8aLOC_Os07g32800Increased when gene overexpression[194]Autophagy-related protein
      OsPIN9LOC_Os01g58860Unknown[195]Auxin efflux transporter
      OsNLP4LOC_Os09g37710Unknown[196,197]NIN-like protein
      OsNLP3LOC_Os01g13540Unknown[198]NIN-like protein
      OsNLP1LOC_Os03g03900Unknown[199]NIN-like protein
      OsAAP6/qPC1LOC_Os01g65670Increased when gene overexpression[25]Amino acid permease
      OsAAP10LOC_Os02g49060Decreased when gene knock out[200]Amino acid permease
      OsAAP5LOC_Os01g65660Unknown[201]Amino acid permease
      OsAAP3LOC_Os06g36180Increased when gene overexpression[202]Amino acid permease
      OsAAP1LOC_Os07g04180Increased when gene overexpression and decreased when gene interference[203]Amino acid permease
      OsAMT1;1/OsAMT1-1LOC_Os04g43070Unknown[204]High-affinity ammonium transporter
      OsAMT2;1LOC_Os05g39240Unknown[205]Ammonium transporter
      OsGS1/OsGS1;1/OsGLN1;1/λGS28LOC_Os02g50240Decreased when OsGS1;1b overexpression[206]Glutamine synthetase
      OsGS2/OsGLN2/λGS31LOC_Os04g56400Increased when concurrent overexpression of OsGS1 and OsGS2[207]Glutamine synthetase
      OsAMT1;3/OsAMT1.3/OsAMT1;2LOC_Os02g40710Increased when gene overexpression[208]Ammonium transporter
      OsGOGAT1LOC_Os01g48960Increased when gene overexpression[208]Glutamate synthetase 1
      OsAS1/ OsASN1LOC_Os03g18130Increased when gene overexpression[209]Asparagine synthetase
      OsSHM1/OsSHMT1LOC_Os03g52840Unknown[210]Serine hydroxymethyltransferase 1
      OsENOD93-1LOC_Os06g05010Unknown[211]Early nodulin 93 ENOD93 protein
      OsNRT2.3/OsNRT2.3a/OsNRT2.3bLOC_Os01g50820Unknown[212]High-affinity nitrate transporter
      OsNAR2.1LOC_Os02g38230Unknown[213]Partner protein for high-affinity nitrate transport
      OsNRT2.1LOC_Os02g02170Unknown[214]High-affinity nitrate transporter
      OsNRT1.1A/OsNPF6.3LOC_Os08g05910Unknown[215]Nitrate transporter
      DNR1LOC_Os01g08270Decreased when gene knock out[216]Amino transferase
      qSBM1LOC_Os01g65120Unknown[217]Peptide transporter
      OsRBCS2LOC_Os12g17600Unknown[218]Small subunit of Rubisco
      OSA1LOC_Os03g48310Unknown[219]Plasma membrane H+-ATPase
      OsDREB1CLOC_Os06g03670Increased when gene overexpression[111]AP2/EREBP transcription factor
      OsPTR6/OsNPF7.3LOC_Os04g50950Unknown[220]Peptide transporter
      OsMADS1/LHS1/AFO/LGY3/GW3p6LOC_Os03g11614Unknown[221,222]MADS-domain transcription factor
    • Rice protein content plays a key role in determining the cooking and eating quality of rice. A high protein content tends to make rice grains compact, resulting in poor water absorption and greatly reducing the taste of rice. Therefore, in production practice, reducing the protein content in rice is helpful for improving the cooking and eating qualities of rice. Although research on breeding rice with proper protein content has been conducted for many years, there are currently no effective methods in production practice to regulate rice protein content and improve the cooking and eating qualities of rice. Hybrid breeding is the most commonly used method for quality breeding worldwide[112]. For rice quality traits that exhibit relatively simple genetic behavior, germplasm resources with excellent rice quality traits can be selected and improved by crossbreeding. Some well-known high-quality varieties, such as Koshihikari from Japan, Basmati370 from the United States, IR64 from the International Rice Research Institute, and Daohuaxiang 2 from China, are bred through hybridization. However, for protein content, a typical quantitative trait controlled by multiple genes, the genetic basis is complex and greatly affected by environmental factors, making it challenging to achieve ideal improvement using traditional hybrid breeding.

      It may be effective to improve the quality traits of rice using physical and chemical factors to induce variation. Schaeffer & Sharpe performed biochemical mutagenesis by increasing the contents of lysine, threonine, and cysteine in the culture medium and obtained mutant lines with high lysine content in rice through cell culture[113,114].

      It is also a good choice for collecting a wide range of germplasm resources, selecting varieties with specific traits, and improving them to meet human needs. Juliano et al. screened 38 rice varieties with lysine content 0.5% higher than the average level of 10,493 rice varieties[115]. Mochizuki & Hara used the low-gluten material NM67 to breed a rice variety LGC-1 with significantly reduced absorbable glutelin, and the content of prolamin in the rice that cannot be absorbed by the human body is high[116]. By crossing LGC-1 with Wuyujing 3, combined with breeding for agronomic traits and molecular marker-assisted selection, Zhang et al. obtained three new rice varieties with excellent agronomic traits and glutelin content close to that of LGC-1[117].

      Since the 1990s, the continuous development of molecular biology technology has created good conditions for the genetic improvement of rice quality, and progress has been made in the creation of high-quality rice materials and rice quality breeding using biotechnology. The application of transgenic technology to introduce exogenous special genes and express them efficiently may be an effective strategy for increasing the content of essential amino acids in rice. Lee et al. carried out point mutations in the maize dhps gene and connected the gene to the promoter of CsMV35S and GluB-1, respectively, to transform and obtain transgenic rice, and the lysine content in mature seeds was significantly increased[118]. Liu et al. linked the endosperm-specific expression promoter to lysine-rich foreign proteins, which also increased the lysine content of seeds by 30%[119]. A sulfur-rich storage protein gene from sesame was transferred into rice and expressed, which simultaneously increased cysteine and methionine in the endosperm and total protein content at the same time[120]. The transfer of sulfur-rich genes from sunflower to rice could also increase cysteine and methionine levels in the endosperm; however, the total protein content decreased[121]. Zhou et al. transformed the aspartate aminotransferase gene from Escherichia coli into rice, which increased the content of amino acids and proteins in rice[122]. The OASA1D gene, encoding a feedback-insensitive α-subunit of rice anthranilate synthase, was expressed in rice driven by the maize ubiquitin promoter, which increased the content of tryptophan in seeds[123].

      The 3' untranslated region regulates gene expression at the transcriptional and post-transcriptional levels by affecting the accumulation, stability, and translation efficiency of mRNA[124126]. Li et al. evaluated the 3'-UTRs of nine seed storage protein (SSP) genes as terminators to enhance glutelin GluB-3 promoter-driven β-glucuronidase (gus A) reporter gene expression in stable transgenic rice lines, in which six 3'-UTRs significantly enhanced the activity of the GluB-3 promoter without altering its tissue specificity[127]. Yang et al. found that transgenic seeds using the 3' UTR of GluB-1 as the terminator had more accumulation of the target expression protein than transgenic seeds using the Nos terminator[128]. These results indicate that it is feasible to regulate the key genes of protein content at the transcription and translation levels using genetic engineering.

      In recent years, the popularity of gene-editing technology has provided an opportunity to improve the protein content of rice. Yang et al. used Crispr-cas9 technology to edit eight members of the glutelin gene family and obtained seven different homozygous mutation types, including double, triple, quadruple, quintuple, and sextuple mutants. Notably, type II, III, IV, V, and VI mutants with moderately reduced grain protein content significantly increased the rice taste value, improved its appearance, and decreased hardness[57]. Similarly, Chen et al. designed three sgRNAs targeting nine glutelin genes and generated nine T-DNA-free homozygous editing lines that exhibited reduced glutelin content compared with the wild type. These low glutelin lines all showed agronomic traits similar to the wild type, including yield components and viscosity characteristics[129].

    • The cooking and eating qualities of rice may differ among different individuals. Thousands of rice varieties vary in cooking taste, particularly in texture. This highly significant trait in rice has attracted the attention of scientists for nearly three-quarters of a century and has only recently begun to be fully understood. An increasing number of studies have shown that grain protein is the most important factor affecting cooking and eating quality after starch. However, more research is needed to fully understand the relationship between grain protein and rice quality, as well as to develop strategies for optimizing it to meet human dietary needs. Therefore, it can be strengthened in the following aspects:

      1. Enhancing the genetic mechanism of protein content in rice.

      Rice protein content is a typical quantitative trait. Although hundreds of QTLs affecting rice grain protein content have been identified, only two genes regulating protein content have been cloned, both of which are positive regulators of protein content. Further new genes regulating protein content in rice need to be further explored. The formation of rice storage proteins is a complex process involving nitrogen absorption, transport, assimilation, distribution, reuse, amino acid synthesis, amino acid modification, amino acid transport, protein synthesis, transport, modification, storage, and degradation. The molecular genetic mechanisms of each step need to be further analyzed.

      2. Strengthen study on the mechanism of the effect of protein on eating quality.

      A series of physical and chemical changes occur in rice during cooking, including water absorption of rice grains, gelatinization of starch, dissolution of starch after endosperm cell breakage, and formation of adhesion layers. In this process, whether the protein itself has an indirect effect on the taste or a direct effect on the water absorption of rice grains, starch gelatinization, and expansion, the type of extract, and the thickness of the adhesive layer, the specific mechanism needs to be further explored. In addition, the interactions among the proteins, starch, and lipid require further clarification. In summary, an in-depth study on the relationship between rice protein, cooking, and eating quality will provide a scientific basis for breeders to select and cultivate varieties with superior tastes.

      3. Rational application of nitrogen fertilizer and breeding of varieties with high nitrogen efficiency.

      Although nitrogen fertilizer is commonly used to increase rice yield, its inefficient use not only causes environmental pollution but also results to an increase in protein content in rice. This excessive use of nitrogen fertilizer leads to the deterioration of cooking and eating quality of rice. Exploring more nitrogen-efficient genes and analyzing the mechanism of their influence on protein content in rice will help cultivate nitrogen-efficient varieties. This, in turn, will lead to synergistic improvement in rice yield and quality, with minimal nitrogen fertilizer usage.

    • The authors confirm contribution to the paper as follows: study conception and design: Lou G, He Y; data collection: Lou G, Bhat M, Tan X, Wang Y; draft manuscript preparation: Lou G, He Y. All authors reviewed the results and approved the final version of the manuscript.

    • Data sharing not applicable to this article as no datasets were generated or analyzed during the current study.

      • This work was supported by grants from the National Natural Science Foundation of China (U21A20211, 31821005), AgroST Project (NK20220501) and China Agriculture Research System (CARS-01-01).

      • The authors declare that they have no conflict of interest.

      • Copyright: © 2023 by the author(s). Published by Maximum Academic Press on behalf of Hainan Yazhou Bay Seed Laboratory. This article is an open access article distributed under Creative Commons Attribution License (CC BY 4.0), visit https://creativecommons.org/licenses/by/4.0/.
    Figure (3)  Table (2) References (222)
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    Lou G, Bhat MA, Tan X, Wang Y, He Y. 2023. Research progress on the relationship between rice protein content and cooking and eating quality and its influencing factors. Seed Biology 2:16 doi: 10.48130/SeedBio-2023-0016
    Lou G, Bhat MA, Tan X, Wang Y, He Y. 2023. Research progress on the relationship between rice protein content and cooking and eating quality and its influencing factors. Seed Biology 2:16 doi: 10.48130/SeedBio-2023-0016

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